diff --git a/cmd/fleetctl/fleetctl/generate_gitops.go b/cmd/fleetctl/fleetctl/generate_gitops.go
index 3a9ddfb7b6..496b08944a 100644
--- a/cmd/fleetctl/fleetctl/generate_gitops.go
+++ b/cmd/fleetctl/fleetctl/generate_gitops.go
@@ -1388,7 +1388,7 @@ func (cmd *GenerateGitopsCommand) generateScripts(teamId *uint, teamName string)
 	// Get scripts.
 	query := ""
 	if teamId != nil {
-		query = fmt.Sprintf("team_id=%d", *teamId)
+		query = fmt.Sprintf("fleet_id=%d", *teamId)
 	}
 	scripts, err := cmd.Client.ListScripts(query)
 	if err != nil {
@@ -1568,7 +1568,7 @@ func (cmd *GenerateGitopsCommand) generateSoftware(filePath string, teamID uint,
 		return nil, nil // software is premium-only
 	}
 
-	query := fmt.Sprintf("available_for_install=1&team_id=%d", teamID)
+	query := fmt.Sprintf("available_for_install=1&fleet_id=%d", teamID)
 	software, err := cmd.Client.ListSoftwareTitles(query)
 	if err != nil {
 		fmt.Fprintf(cmd.CLI.App.ErrWriter, "Error getting software: %s\n", err)
diff --git a/cmd/fleetctl/fleetctl/generate_gitops_test.go b/cmd/fleetctl/fleetctl/generate_gitops_test.go
index 7f2c876920..79d2f86e1d 100644
--- a/cmd/fleetctl/fleetctl/generate_gitops_test.go
+++ b/cmd/fleetctl/fleetctl/generate_gitops_test.go
@@ -98,23 +98,23 @@ func (c *MockClient) ListTeams(query string) ([]fleet.Team, error) {
 
 func (MockClient) ListScripts(query string) ([]*fleet.Script, error) {
 	switch query {
-	case "team_id=1":
+	case "fleet_id=1":
 		return []*fleet.Script{{
 			ID:              2,
 			TeamID:          ptr.Uint(1),
 			Name:            "Script B.ps1",
 			ScriptContentID: 2,
 		}}, nil
-	case "team_id=0":
+	case "fleet_id=0":
 		return []*fleet.Script{{
 			ID:              3,
 			TeamID:          ptr.Uint(0),
 			Name:            "Script Z.ps1",
 			ScriptContentID: 3,
 		}}, nil
-	case "team_id=2", "team_id=3", "team_id=4", "team_id=5":
+	case "fleet_id=2", "fleet_id=3", "fleet_id=4", "fleet_id=5":
 		return nil, nil
-	case "team_id=6":
+	case "fleet_id=6":
 		return nil, nil
 	default:
 		return nil, fmt.Errorf("unexpected query: %s", query)
@@ -249,7 +249,7 @@ func (MockClient) GetTeam(teamID uint) (*fleet.Team, error) {
 
 func (MockClient) ListSoftwareTitles(query string) ([]fleet.SoftwareTitleListResult, error) {
 	switch query {
-	case "available_for_install=1&team_id=1":
+	case "available_for_install=1&fleet_id=1":
 		return []fleet.SoftwareTitleListResult{
 			{
 				ID:         1,
@@ -312,7 +312,7 @@ func (MockClient) ListSoftwareTitles(query string) ([]fleet.SoftwareTitleListRes
 				},
 			},
 		}, nil
-	case "available_for_install=1&team_id=0":
+	case "available_for_install=1&fleet_id=0":
 		return []fleet.SoftwareTitleListResult{}, nil
 	default:
 		return nil, fmt.Errorf("unexpected query: %s", query)
@@ -1592,7 +1592,7 @@ type MockClientWithScriptPackage struct {
 
 func (c *MockClientWithScriptPackage) ListSoftwareTitles(query string) ([]fleet.SoftwareTitleListResult, error) {
 	switch query {
-	case "available_for_install=1&team_id=2":
+	case "available_for_install=1&fleet_id=2":
 		return []fleet.SoftwareTitleListResult{
 			{
 				ID:         3,
diff --git a/cmd/fleetctl/fleetctl/get.go b/cmd/fleetctl/fleetctl/get.go
index fc81bd8c6a..21384cb464 100644
--- a/cmd/fleetctl/fleetctl/get.go
+++ b/cmd/fleetctl/fleetctl/get.go
@@ -884,7 +884,7 @@ func getHostsCommand() *cli.Command {
 				query := url.Values{}
 				query.Set("additional_info_filters", "*")
 				if teamID := c.Uint(fleetFlagName); teamID > 0 {
-					query.Set("team_id", strconv.FormatUint(uint64(teamID), 10))
+					query.Set("fleet_id", strconv.FormatUint(uint64(teamID), 10))
 				}
 
 				if c.Bool("mdm") || c.Bool("mdm-pending") {
@@ -1306,7 +1306,7 @@ func getSoftwareCommand() *cli.Command {
 
 			teamID := c.Uint(fleetFlagName)
 			if teamID != 0 {
-				query.Set("team_id", strconv.FormatUint(uint64(teamID), 10))
+				query.Set("fleet_id", strconv.FormatUint(uint64(teamID), 10))
 			}
 
 			if c.Bool("versions") {
diff --git a/ee/server/service/in_house_apps.go b/ee/server/service/in_house_apps.go
index 610b8ff021..8b67a55aa8 100644
--- a/ee/server/service/in_house_apps.go
+++ b/ee/server/service/in_house_apps.go
@@ -171,7 +171,7 @@ func (svc *Service) GetInHouseAppManifest(ctx context.Context, titleID uint, tea
 		return nil, ctxerr.Wrap(ctx, err, "get in house app manifest: get in house app metadata")
 	}
 
-	downloadURL := fmt.Sprintf("%s/api/latest/fleet/software/titles/%d/in_house_app?team_id=%d", appConfig.ServerSettings.ServerURL, titleID, ptr.ValOrZero(teamID))
+	downloadURL := fmt.Sprintf("%s/api/latest/fleet/software/titles/%d/in_house_app?fleet_id=%d", appConfig.ServerSettings.ServerURL, titleID, ptr.ValOrZero(teamID))
 
 	if svc.config.S3.SoftwareInstallersCloudFrontSigner != nil {
 		signedURL, err := svc.softwareInstallStore.Sign(ctx, meta.StorageID, fleet.InHouseAppSignedURLExpiry)
@@ -184,7 +184,7 @@ func (svc *Service) GetInHouseAppManifest(ctx context.Context, titleID uint, tea
 	}
 
 	// Escape & characters in case of using CloudFront signed URL
-	var funcMap = map[string]any{
+	funcMap := map[string]any{
 		"xml": mobileconfig.XMLEscapeString,
 	}
 
@@ -235,7 +235,6 @@ func (svc *Service) GetInHouseAppManifest(ctx context.Context, titleID uint, tea
 		Name     string
 		URL      string
 	}{meta.BundleIdentifier, meta.Version, meta.SoftwareTitle, downloadURL})
-
 	if err != nil {
 		return nil, ctxerr.Wrap(ctx, err, "rendering app manifest")
 	}
diff --git a/ee/server/service/software_installers_test.go b/ee/server/service/software_installers_test.go
index 4d3230221e..f1e30dd10e 100644
--- a/ee/server/service/software_installers_test.go
+++ b/ee/server/service/software_installers_test.go
@@ -512,7 +512,7 @@ func TestGetInHouseAppManifest(t *testing.T) {
             <key>kind</key>
             <string>software-package</string>
             <key>url</key>
-            <string>https://example.com/api/latest/fleet/software/titles/1/in_house_app?team_id=0</string>
+            <string>https://example.com/api/latest/fleet/software/titles/1/in_house_app?fleet_id=0</string>
           </dict>
           <dict>
             <key>kind</key>
diff --git a/ee/server/service/software_title_icons.go b/ee/server/service/software_title_icons.go
index ab887499b3..e93653cb53 100644
--- a/ee/server/service/software_title_icons.go
+++ b/ee/server/service/software_title_icons.go
@@ -126,7 +126,7 @@ func (svc *Service) UploadSoftwareTitleIcon(ctx context.Context, payload *fleet.
 
 	// if anything on the icon has changed, we need to generate a new activity
 	if icon == nil || icon.StorageID != softwareTitleIcon.StorageID || icon.Filename != softwareTitleIcon.Filename {
-		iconUrl := fmt.Sprintf("/api/latest/fleet/software/titles/%d/icon?team_id=%d", softwareTitleIcon.SoftwareTitleID, softwareTitleIcon.TeamID)
+		iconUrl := softwareTitleIcon.IconUrl()
 		activityDetailsForSoftwareTitleIcon, err := svc.ds.ActivityDetailsForSoftwareTitleIcon(ctxdb.RequirePrimary(ctx, true), payload.TeamID, payload.TitleID)
 		if err != nil {
 			return fleet.SoftwareTitleIcon{}, ctxerr.Wrap(ctx, err, "fetching software title icon activity details")
diff --git a/server/datastore/mysql/activities.go b/server/datastore/mysql/activities.go
index c14508c67b..466dcf9520 100644
--- a/server/datastore/mysql/activities.go
+++ b/server/datastore/mysql/activities.go
@@ -15,9 +15,7 @@ import (
 	"github.com/jmoiron/sqlx"
 )
 
-var (
-	deleteIDsBatchSize = 1000
-)
+var deleteIDsBatchSize = 1000
 
 // ListHostUpcomingActivities returns the list of activities pending execution
 // or processing for the specific host. It is the "unified queue" of work to be
@@ -1487,7 +1485,7 @@ WHERE
 		return ctxerr.Wrap(ctx, err, "get in-house app title id")
 	}
 
-	manifestURL := fmt.Sprintf("%s/api/latest/fleet/software/titles/%d/in_house_app/manifest?team_id=%d", appConfig.ServerSettings.ServerURL, titleID, tid)
+	manifestURL := fmt.Sprintf("%s/api/latest/fleet/software/titles/%d/in_house_app/manifest?fleet_id=%d", appConfig.ServerSettings.ServerURL, titleID, tid)
 
 	// insert the nano command
 	namedArgs := map[string]any{
diff --git a/server/fleet/software_installer_test.go b/server/fleet/software_installer_test.go
index 4f30010fa2..1a4a533bfb 100644
--- a/server/fleet/software_installer_test.go
+++ b/server/fleet/software_installer_test.go
@@ -109,7 +109,7 @@ func TestForMyDevicePage(t *testing.T) {
 		{
 			name: "matching custom icon url",
 			before: func() {
-				iconUrl = ptr.String("/api/latest/fleet/software/titles/42/icon?team_id=7")
+				iconUrl = ptr.String("/api/latest/fleet/software/titles/42/icon?fleet_id=7")
 				hostSoftwareInstaller = HostSoftwareWithInstaller{
 					IconUrl: iconUrl,
 					ID:      1,
diff --git a/server/fleet/software_title_icons.go b/server/fleet/software_title_icons.go
index b502812dee..dae94b8433 100644
--- a/server/fleet/software_title_icons.go
+++ b/server/fleet/software_title_icons.go
@@ -8,7 +8,7 @@ import (
 	"time"
 )
 
-var SoftwareTitleIconURLRegex = regexp.MustCompile(`fleet/software/titles/\d+/icon\?team_id=\d+`)
+var SoftwareTitleIconURLRegex = regexp.MustCompile(`fleet/software/titles/\d+/icon\?(?:team_id|fleet_id)=\d+`)
 
 const SoftwareTitleIconSignedURLExpiry = 6 * time.Hour
 
@@ -37,7 +37,7 @@ func (s *SoftwareTitleIcon) AuthzType() string {
 }
 
 func (s *SoftwareTitleIcon) IconUrl() string {
-	return fmt.Sprintf("/api/latest/fleet/software/titles/%d/icon?team_id=%d", s.SoftwareTitleID, s.TeamID)
+	return fmt.Sprintf("/api/latest/fleet/software/titles/%d/icon?fleet_id=%d", s.SoftwareTitleID, s.TeamID)
 }
 
 func (s *SoftwareTitleIcon) IconUrlWithDeviceToken(deviceToken string) string {
diff --git a/server/platform/endpointer/json_key_rewriter.go b/server/platform/endpointer/json_key_rewriter.go
index c03a1b4ebe..4eae18c8d5 100644
--- a/server/platform/endpointer/json_key_rewriter.go
+++ b/server/platform/endpointer/json_key_rewriter.go
@@ -145,6 +145,20 @@ func RewriteDeprecatedKeys(data []byte, rules []AliasRule) ([]byte, map[string]s
 	return buf.Bytes(), deprecatedKeysMap, nil
 }
 
+// RewriteOldToNewKeys is the reverse of RewriteDeprecatedKey; it takes
+// the rules and reverses them before translating keys.
+// Use this in situations where a payload was rewritten from new to old keys
+// for deserialization, but you want to return a response with the new keys
+// for forward compatibility.
+func RewriteOldToNewKeys(data []byte, rules []AliasRule) ([]byte, error) {
+	reversed := make([]AliasRule, len(rules))
+	for i, r := range rules {
+		reversed[i] = AliasRule{OldKey: r.NewKey, NewKey: r.OldKey}
+	}
+	result, _, err := RewriteDeprecatedKeys(data, reversed)
+	return result, err
+}
+
 // rewrite reads tokens from src, rewrites deprecated keys, checks for alias
 // conflicts, and writes the transformed JSON to w.
 func (r *JSONKeyRewriteReader) rewrite(src io.Reader, w io.Writer) error {
diff --git a/server/platform/endpointer/json_key_rewriter_test.go b/server/platform/endpointer/json_key_rewriter_test.go
index b3ea1c606f..9216aa6938 100644
--- a/server/platform/endpointer/json_key_rewriter_test.go
+++ b/server/platform/endpointer/json_key_rewriter_test.go
@@ -468,3 +468,35 @@ func TestAliasConflictError_ErrorMessage(t *testing.T) {
 	assert.Contains(t, err.Error(), "team_id")
 	assert.Contains(t, err.Error(), "fleet_id")
 }
+
+func TestRewriteOldToNewKeys(t *testing.T) {
+	rules := []AliasRule{
+		{OldKey: "team_id", NewKey: "fleet_id"},
+		{OldKey: "team", NewKey: "fleet"},
+		{OldKey: "custom_settings", NewKey: "configuration_profiles"},
+	}
+
+	t.Run("rewrites old keys to new", func(t *testing.T) {
+		input := `{"team_id":42,"name":"hello","team":"engineering"}`
+		out, err := RewriteOldToNewKeys([]byte(input), rules)
+		require.NoError(t, err)
+
+		var result map[string]any
+		require.NoError(t, json.Unmarshal(out, &result))
+		assert.Equal(t, float64(42), result["fleet_id"])
+		assert.Equal(t, "engineering", result["fleet"])
+		assert.Equal(t, "hello", result["name"])
+		assert.Nil(t, result["team_id"])
+		assert.Nil(t, result["team"])
+	})
+
+	t.Run("new keys pass through unchanged", func(t *testing.T) {
+		input := `{"fleet_id":42}`
+		out, err := RewriteOldToNewKeys([]byte(input), rules)
+		require.NoError(t, err)
+
+		var result map[string]any
+		require.NoError(t, json.Unmarshal(out, &result))
+		assert.Equal(t, float64(42), result["fleet_id"])
+	})
+}
diff --git a/server/service/client.go b/server/service/client.go
index a308f599c0..19c8094126 100644
--- a/server/service/client.go
+++ b/server/service/client.go
@@ -2780,12 +2780,12 @@ func (c *Client) doGitOpsPolicies(config *spec.GitOps, teamSoftwareInstallers []
 		for _, softwareInstaller := range teamSoftwareInstallers {
 			if softwareInstaller.TitleID == nil {
 				// Should not happen, but to not panic we just log a warning.
-				logFn("[!] software installer without title id: team_id=%d, url=%s\n", *teamID, softwareInstaller.URL)
+				logFn("[!] software installer without title id: fleet_id=%d, url=%s\n", *teamID, softwareInstaller.URL)
 				continue
 			}
 			if softwareInstaller.URL == "" && softwareInstaller.HashSHA256 == "" {
 				// Should not happen because we previously applied packages via gitops, but to not panic we just log a warning.
-				logFn("[!] software installer without url: team_id=%d, title_id=%d\n", *teamID, *softwareInstaller.TitleID)
+				logFn("[!] software installer without url: fleet_id=%d, title_id=%d\n", *teamID, *softwareInstaller.TitleID)
 				continue
 			}
 			softwareTitleIDsByInstallerURL[softwareInstaller.URL] = *softwareInstaller.TitleID
@@ -2797,12 +2797,12 @@ func (c *Client) doGitOpsPolicies(config *spec.GitOps, teamSoftwareInstallers []
 			}
 			if vppApp.TitleID == nil {
 				// Should not happen, but to not panic we just log a warning.
-				logFn("[!] VPP app without title id: team_id=%d, app_store_id=%s\n", *teamID, vppApp.AppStoreID)
+				logFn("[!] VPP app without title id: fleet_id=%d, app_store_id=%s\n", *teamID, vppApp.AppStoreID)
 				continue
 			}
 			if vppApp.AppStoreID == "" {
 				// Should not happen because we previously applied apps via gitops, but to not panic we just log a warning.
-				logFn("[!] VPP app without app ID: team_id=%d, title_id=%d\n", *teamID, *vppApp.TitleID)
+				logFn("[!] VPP app without app ID: fleet_id=%d, title_id=%d\n", *teamID, *vppApp.TitleID)
 				continue
 			}
 			softwareTitleIDsByAppStoreAppID[vppApp.AppStoreID] = *vppApp.TitleID
diff --git a/server/service/client_android_certificates.go b/server/service/client_android_certificates.go
index 624ce8ca70..117b0647d4 100644
--- a/server/service/client_android_certificates.go
+++ b/server/service/client_android_certificates.go
@@ -8,7 +8,7 @@ import (
 func (c *Client) GetCertificateTemplates(teamID string) ([]*fleet.CertificateTemplateResponseSummary, error) {
 	verb, path := "GET", "/api/latest/fleet/certificates"
 	var responseBody listCertificateTemplatesResponse
-	query := "team_id=" + teamID
+	query := "fleet_id=" + teamID
 	err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query)
 	if err != nil {
 		return nil, err
diff --git a/server/service/client_appconfig.go b/server/service/client_appconfig.go
index 6c561da044..ab5627619b 100644
--- a/server/service/client_appconfig.go
+++ b/server/service/client_appconfig.go
@@ -1,7 +1,10 @@
 package service
 
 import (
+	"encoding/json"
+
 	"github.com/fleetdm/fleet/v4/server/fleet"
+	"github.com/fleetdm/fleet/v4/server/platform/endpointer"
 	"github.com/fleetdm/fleet/v4/server/version"
 )
 
@@ -9,7 +12,15 @@ import (
 func (c *Client) ApplyAppConfig(payload interface{}, opts fleet.ApplySpecOptions) error {
 	verb, path := "PATCH", "/api/latest/fleet/config"
 	var responseBody appConfigResponse
-	return c.authenticatedRequestWithQuery(payload, verb, path, &responseBody, opts.RawQuery())
+	data, err := json.Marshal(payload)
+	if err != nil {
+		return err
+	}
+	data, err = endpointer.RewriteOldToNewKeys(data, endpointer.ExtractAliasRules(fleet.AppConfig{}))
+	if err != nil {
+		return err
+	}
+	return c.authenticatedRequestWithQuery(data, verb, path, &responseBody, opts.RawQuery())
 }
 
 // ApplyNoTeamProfiles sends the list of profiles to be applied for the hosts
diff --git a/server/service/client_labels.go b/server/service/client_labels.go
index e937047762..a1343e1a79 100644
--- a/server/service/client_labels.go
+++ b/server/service/client_labels.go
@@ -24,7 +24,7 @@ func (c *Client) ApplyLabels(
 			verb,
 			path,
 			&responseBody,
-			fmt.Sprintf("team_id=%d", *teamID),
+			fmt.Sprintf("fleet_id=%d", *teamID),
 		)
 	}
 	return c.authenticatedRequest(req, verb, path, &responseBody)
@@ -42,7 +42,7 @@ func (c *Client) GetLabel(name string) (*fleet.LabelSpec, error) {
 func (c *Client) GetLabels(teamID uint) ([]*fleet.LabelSpec, error) {
 	verb, path := "GET", "/api/latest/fleet/spec/labels"
 	var responseBody getLabelSpecsResponse
-	err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, fmt.Sprintf("team_id=%d", teamID))
+	err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, fmt.Sprintf("fleet_id=%d", teamID))
 	return responseBody.Specs, err
 }
 
diff --git a/server/service/client_live_query.go b/server/service/client_live_query.go
index 6b7fe54605..9fa297bfb2 100644
--- a/server/service/client_live_query.go
+++ b/server/service/client_live_query.go
@@ -74,7 +74,7 @@ func (c *Client) LiveQueryWithContext(
 		QuerySQL: query,
 		Selected: distributedQueryCampaignTargetsByIdentifiers{Labels: labels, Hosts: hostIdentifiers},
 	}
-	verb, path := "POST", "/api/latest/fleet/queries/run_by_identifiers"
+	verb, path := "POST", "/api/latest/fleet/reports/run_by_identifiers"
 	var responseBody createDistributedQueryCampaignResponse
 	err := c.authenticatedRequest(req, verb, path, &responseBody)
 	if err != nil {
diff --git a/server/service/client_live_query_test.go b/server/service/client_live_query_test.go
index f797c025b6..bf6726bce2 100644
--- a/server/service/client_live_query_test.go
+++ b/server/service/client_live_query_test.go
@@ -20,7 +20,7 @@ func TestLiveQueryWithContext(t *testing.T) {
 	upgrader := websocket.Upgrader{}
 	ts := httptest.NewServer(http.HandlerFunc(func(w http.ResponseWriter, r *http.Request) {
 		switch r.URL.Path {
-		case "/api/latest/fleet/queries/run_by_identifiers":
+		case "/api/latest/fleet/reports/run_by_identifiers":
 			resp := createDistributedQueryCampaignResponse{
 				Campaign: &fleet.DistributedQueryCampaign{
 					UpdateCreateTimestamps: fleet.UpdateCreateTimestamps{
diff --git a/server/service/client_mdm.go b/server/service/client_mdm.go
index a722325f06..3a5b9d85ec 100644
--- a/server/service/client_mdm.go
+++ b/server/service/client_mdm.go
@@ -116,8 +116,8 @@ func (c *Client) UploadBootstrapPackage(pkg *fleet.MDMAppleBootstrapPackage, dry
 		return err
 	}
 
-	// add the team_id field
-	if err := w.WriteField("team_id", fmt.Sprint(pkg.TeamID)); err != nil {
+	// add the fleet_id field
+	if err := w.WriteField("fleet_id", fmt.Sprint(pkg.TeamID)); err != nil {
 		return err
 	}
 
diff --git a/server/service/client_policies.go b/server/service/client_policies.go
index 388d7d80d9..858ca00c73 100644
--- a/server/service/client_policies.go
+++ b/server/service/client_policies.go
@@ -1,9 +1,11 @@
 package service
 
 import (
+	"encoding/json"
 	"fmt"
 
 	"github.com/fleetdm/fleet/v4/server/fleet"
+	"github.com/fleetdm/fleet/v4/server/platform/endpointer"
 )
 
 func (c *Client) CreateGlobalPolicy(name, query, description, resolution, platform string) error {
@@ -25,14 +27,22 @@ func (c *Client) ApplyPolicies(specs []*fleet.PolicySpec) error {
 	req := applyPolicySpecsRequest{Specs: specs}
 	verb, path := "POST", "/api/latest/fleet/spec/policies"
 	var responseBody applyPolicySpecsResponse
-	return c.authenticatedRequest(req, verb, path, &responseBody)
+	data, err := json.Marshal(req)
+	if err != nil {
+		return err
+	}
+	data, err = endpointer.RewriteOldToNewKeys(data, endpointer.ExtractAliasRules(req))
+	if err != nil {
+		return err
+	}
+	return c.authenticatedRequest(data, verb, path, &responseBody)
 }
 
 // GetPolicies retrieves the list of Policies. Inherited policies are excluded.
 func (c *Client) GetPolicies(teamID *uint) ([]*fleet.Policy, error) {
 	verb, path := "GET", ""
 	if teamID != nil {
-		path = fmt.Sprintf("/api/latest/fleet/teams/%d/policies", *teamID)
+		path = fmt.Sprintf("/api/latest/fleet/fleets/%d/policies", *teamID)
 	} else {
 		path = "/api/latest/fleet/policies"
 	}
@@ -50,7 +60,7 @@ func (c *Client) DeletePolicies(teamID *uint, ids []uint) error {
 	verb, path := "POST", ""
 	req := deleteTeamPoliciesRequest{IDs: ids}
 	if teamID != nil {
-		path = fmt.Sprintf("/api/latest/fleet/teams/%d/policies/delete", *teamID)
+		path = fmt.Sprintf("/api/latest/fleet/fleets/%d/policies/delete", *teamID)
 		req.TeamID = *teamID
 	} else {
 		path = "/api/latest/fleet/policies/delete"
diff --git a/server/service/client_profiles.go b/server/service/client_profiles.go
index ca80df870d..5962fba628 100644
--- a/server/service/client_profiles.go
+++ b/server/service/client_profiles.go
@@ -27,7 +27,7 @@ func (c *Client) ListProfiles(teamID *uint) ([]*fleet.MDMAppleConfigProfile, err
 	verb, path := "GET", "/api/latest/fleet/mdm/apple/profiles"
 	query := make(url.Values)
 	if teamID != nil {
-		query.Add("team_id", strconv.FormatUint(uint64(*teamID), 10))
+		query.Add("fleet_id", strconv.FormatUint(uint64(*teamID), 10))
 	}
 	var responseBody listMDMAppleConfigProfilesResponse
 	if err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query.Encode()); err != nil {
@@ -40,7 +40,7 @@ func (c *Client) ListConfigurationProfiles(teamID *uint) ([]*fleet.MDMConfigProf
 	verb, path := "GET", "/api/latest/fleet/configuration_profiles"
 	query := make(url.Values)
 	if teamID != nil {
-		query.Add("team_id", strconv.FormatUint(uint64(*teamID), 10))
+		query.Add("fleet_id", strconv.FormatUint(uint64(*teamID), 10))
 	}
 	var responseBody listMDMConfigProfilesResponse
 	if err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query.Encode()); err != nil {
@@ -77,7 +77,7 @@ func (c *Client) AddProfile(teamID uint, configurationProfile []byte) (uint, err
 	}
 	body := &bytes.Buffer{}
 	writer := multipart.NewWriter(body)
-	teamIDField, err := writer.CreateFormField("team_id")
+	teamIDField, err := writer.CreateFormField("fleet_id")
 	if err != nil {
 		return 0, err
 	}
@@ -138,7 +138,7 @@ func (c *Client) GetConfigProfilesSummary(teamID *uint) (*fleet.MDMProfilesSumma
 	verb, path := "GET", "/api/latest/fleet/mdm/profiles/summary"
 	query := make(url.Values)
 	if teamID != nil {
-		query.Add("team_id", strconv.FormatUint(uint64(*teamID), 10))
+		query.Add("fleet_id", strconv.FormatUint(uint64(*teamID), 10))
 	}
 	var responseBody getMDMProfilesSummaryResponse
 	if err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query.Encode()); err != nil {
@@ -152,7 +152,7 @@ func (c *Client) GetAppleMDMEnrollmentProfile(teamID uint) (*fleet.MDMAppleSetup
 	verb, path := "GET", "/api/latest/fleet/enrollment_profiles/automatic"
 	var query string
 	if teamID != 0 {
-		query = fmt.Sprintf("team_id=%d", teamID)
+		query = fmt.Sprintf("fleet_id=%d", teamID)
 	}
 	var responseBody createMDMAppleSetupAssistantResponse
 	if err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query); err != nil {
diff --git a/server/service/client_queries.go b/server/service/client_queries.go
index 0870482632..502bc33560 100644
--- a/server/service/client_queries.go
+++ b/server/service/client_queries.go
@@ -1,27 +1,37 @@
 package service
 
 import (
+	"encoding/json"
 	"fmt"
 	"net/url"
 
 	"github.com/fleetdm/fleet/v4/server/fleet"
+	"github.com/fleetdm/fleet/v4/server/platform/endpointer"
 )
 
 // ApplyQueries sends the list of Queries to be applied (upserted) to the
 // Fleet instance.
 func (c *Client) ApplyQueries(specs []*fleet.QuerySpec) error {
 	req := applyQuerySpecsRequest{Specs: specs}
-	verb, path := "POST", "/api/latest/fleet/spec/queries"
+	verb, path := "POST", "/api/latest/fleet/spec/reports"
 	var responseBody applyQuerySpecsResponse
-	return c.authenticatedRequest(req, verb, path, &responseBody)
+	data, err := json.Marshal(req)
+	if err != nil {
+		return err
+	}
+	data, err = endpointer.RewriteOldToNewKeys(data, endpointer.ExtractAliasRules(req))
+	if err != nil {
+		return err
+	}
+	return c.authenticatedRequest(data, verb, path, &responseBody)
 }
 
 // GetQuerySpec returns the query spec of a query by its team+name.
 func (c *Client) GetQuerySpec(teamID *uint, name string) (*fleet.QuerySpec, error) {
-	verb, path := "GET", "/api/latest/fleet/spec/queries/"+url.PathEscape(name)
+	verb, path := "GET", "/api/latest/fleet/spec/reports/"+url.PathEscape(name)
 	query := url.Values{}
 	if teamID != nil {
-		query.Set("team_id", fmt.Sprint(*teamID))
+		query.Set("fleet_id", fmt.Sprint(*teamID))
 	}
 	var responseBody getQuerySpecResponse
 	err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query.Encode())
@@ -30,10 +40,10 @@ func (c *Client) GetQuerySpec(teamID *uint, name string) (*fleet.QuerySpec, erro
 
 // GetQueries retrieves the list of all Queries.
 func (c *Client) GetQueries(teamID *uint, name *string) ([]fleet.Query, error) {
-	verb, path := "GET", "/api/latest/fleet/queries"
+	verb, path := "GET", "/api/latest/fleet/reports"
 	query := url.Values{}
 	if teamID != nil {
-		query.Set("team_id", fmt.Sprint(*teamID))
+		query.Set("fleet_id", fmt.Sprint(*teamID))
 	}
 	if name != nil {
 		query.Set("query", *name)
@@ -48,7 +58,7 @@ func (c *Client) GetQueries(teamID *uint, name *string) ([]fleet.Query, error) {
 
 // DeleteQuery deletes the query with the matching name.
 func (c *Client) DeleteQuery(name string) error {
-	verb, path := "DELETE", "/api/latest/fleet/queries/"+url.PathEscape(name)
+	verb, path := "DELETE", "/api/latest/fleet/reports/"+url.PathEscape(name)
 	var responseBody deleteQueryResponse
 	return c.authenticatedRequest(nil, verb, path, &responseBody)
 }
@@ -56,7 +66,7 @@ func (c *Client) DeleteQuery(name string) error {
 // DeleteQueries deletes several queries.
 func (c *Client) DeleteQueries(ids []uint) error {
 	req := deleteQueriesRequest{IDs: ids}
-	verb, path := "POST", "/api/latest/fleet/queries/delete"
+	verb, path := "POST", "/api/latest/fleet/reports/delete"
 	var responseBody deleteQueriesResponse
 	return c.authenticatedRequest(req, verb, path, &responseBody)
 }
diff --git a/server/service/client_scripts.go b/server/service/client_scripts.go
index cafd07c68a..7b9a42cfbf 100644
--- a/server/service/client_scripts.go
+++ b/server/service/client_scripts.go
@@ -159,7 +159,7 @@ func (c *Client) validateMacOSSetupScript(fileName string) ([]byte, error) {
 func (c *Client) deleteMacOSSetupScript(teamID *uint) error {
 	var query string
 	if teamID != nil {
-		query = fmt.Sprintf("team_id=%d", *teamID)
+		query = fmt.Sprintf("fleet_id=%d", *teamID)
 	}
 
 	verb, path := "DELETE", "/api/latest/fleet/setup_experience/script"
@@ -181,9 +181,9 @@ func (c *Client) uploadMacOSSetupScript(filename string, data []byte, teamID *ui
 		return err
 	}
 
-	// add the team_id field
+	// add the fleet_id field
 	if teamID != nil {
-		if err := w.WriteField("team_id", fmt.Sprint(*teamID)); err != nil {
+		if err := w.WriteField("fleet_id", fmt.Sprint(*teamID)); err != nil {
 			return err
 		}
 	}
@@ -248,7 +248,7 @@ func (c *Client) GetSetupExperienceScript(teamID uint) (*fleet.Script, error) {
 	verb, path := "GET", "/api/latest/fleet/setup_experience/script"
 	var query string
 	if teamID != 0 {
-		query = fmt.Sprintf("team_id=%d", teamID)
+		query = fmt.Sprintf("fleet_id=%d", teamID)
 	}
 	var responseBody getSetupExperienceScriptResponse
 	err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query)
diff --git a/server/service/client_software.go b/server/service/client_software.go
index 16156f64ed..b0e5145827 100644
--- a/server/service/client_software.go
+++ b/server/service/client_software.go
@@ -40,7 +40,7 @@ func (c *Client) ListSoftwareTitles(query string) ([]fleet.SoftwareTitleListResu
 func (c *Client) GetSetupExperienceSoftware(platform string, teamID uint) ([]fleet.SoftwareTitleListResult, error) {
 	verb, path := "GET", "/api/latest/fleet/setup_experience/software"
 	var responseBody getSetupExperienceSoftwareResponse
-	query := fmt.Sprintf("platform=%s&team_id=%d", platform, teamID)
+	query := fmt.Sprintf("platform=%s&fleet_id=%d", platform, teamID)
 	err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query)
 	if err != nil {
 		return nil, err
@@ -54,7 +54,7 @@ func (c *Client) GetSetupExperienceSoftware(platform string, teamID uint) ([]fle
 func (c *Client) GetSoftwareTitleByID(ID uint, teamID *uint) (*fleet.SoftwareTitle, error) {
 	var query string
 	if teamID != nil {
-		query = fmt.Sprintf("team_id=%d", *teamID)
+		query = fmt.Sprintf("fleet_id=%d", *teamID)
 	}
 	verb, path := "GET", "/api/latest/fleet/software/titles/"+fmt.Sprint(ID)
 	var responseBody getSoftwareTitleResponse
@@ -67,7 +67,7 @@ func (c *Client) GetSoftwareTitleByID(ID uint, teamID *uint) (*fleet.SoftwareTit
 
 func (c *Client) GetSoftwareTitleIcon(titleID uint, teamID uint) ([]byte, error) {
 	verb, path := "GET", fmt.Sprintf("/api/latest/fleet/software/titles/%d/icon", titleID)
-	response, err := c.AuthenticatedDo(verb, path, fmt.Sprintf("team_id=%d", teamID), nil)
+	response, err := c.AuthenticatedDo(verb, path, fmt.Sprintf("fleet_id=%d", teamID), nil)
 	if err != nil {
 		return nil, fmt.Errorf("%s %s: %w", verb, path, err)
 	}
@@ -211,7 +211,7 @@ func (c *Client) putIcon(teamID uint, titleID uint, writer *multipart.Writer, bu
 		context.Background(),
 		"PUT",
 		fmt.Sprintf("/api/latest/fleet/software/titles/%d/icon", titleID),
-		fmt.Sprintf("team_id=%d", teamID),
+		fmt.Sprintf("fleet_id=%d", teamID),
 		buf.Bytes(),
 		map[string]string{
 			"Content-Type":  writer.FormDataContentType(),
@@ -235,7 +235,7 @@ func (c *Client) DeleteIcon(teamID uint, titleID uint) error {
 	response, err := c.AuthenticatedDo(
 		"DELETE",
 		fmt.Sprintf("/api/latest/fleet/software/titles/%d/icon", titleID),
-		fmt.Sprintf("team_id=%d", teamID),
+		fmt.Sprintf("fleet_id=%d", teamID),
 		nil,
 	)
 	if err != nil {
diff --git a/server/service/client_teams.go b/server/service/client_teams.go
index ba46171414..dab2e36866 100644
--- a/server/service/client_teams.go
+++ b/server/service/client_teams.go
@@ -7,11 +7,12 @@ import (
 	"strconv"
 
 	"github.com/fleetdm/fleet/v4/server/fleet"
+	"github.com/fleetdm/fleet/v4/server/platform/endpointer"
 )
 
 // ListTeams retrieves the list of teams.
 func (c *Client) ListTeams(query string) ([]fleet.Team, error) {
-	verb, path := "GET", "/api/latest/fleet/teams"
+	verb, path := "GET", "/api/latest/fleet/fleets"
 	var responseBody listTeamsResponse
 	err := c.authenticatedRequestWithQuery(nil, verb, path, &responseBody, query)
 	if err != nil {
@@ -25,7 +26,7 @@ func (c *Client) CreateTeam(teamPayload fleet.TeamPayload) (*fleet.Team, error)
 	req := createTeamRequest{
 		TeamPayload: teamPayload,
 	}
-	verb, path := "POST", "/api/latest/fleet/teams"
+	verb, path := "POST", "/api/latest/fleet/fleets"
 	var responseBody teamResponse
 	err := c.authenticatedRequest(req, verb, path, &responseBody)
 	if err != nil {
@@ -35,7 +36,7 @@ func (c *Client) CreateTeam(teamPayload fleet.TeamPayload) (*fleet.Team, error)
 }
 
 func (c *Client) GetTeam(teamID uint) (*fleet.Team, error) {
-	verb, path := "GET", fmt.Sprintf("/api/latest/fleet/teams/%d", teamID)
+	verb, path := "GET", fmt.Sprintf("/api/latest/fleet/fleets/%d", teamID)
 	var responseBody getTeamResponse
 	if err := c.authenticatedRequest(nil, verb, path, &responseBody); err != nil {
 		return nil, err
@@ -45,7 +46,7 @@ func (c *Client) GetTeam(teamID uint) (*fleet.Team, error) {
 
 // DeleteTeam deletes a team.
 func (c *Client) DeleteTeam(teamID uint) error {
-	verb, path := "DELETE", "/api/latest/fleet/teams/"+strconv.FormatUint(uint64(teamID), 10)
+	verb, path := "DELETE", "/api/latest/fleet/fleets/"+strconv.FormatUint(uint64(teamID), 10)
 	var responseBody deleteTeamResponse
 	return c.authenticatedRequest(nil, verb, path, &responseBody)
 }
@@ -53,9 +54,19 @@ func (c *Client) DeleteTeam(teamID uint) error {
 // ApplyTeams sends the list of Teams to be applied to the
 // Fleet instance.
 func (c *Client) ApplyTeams(specs []json.RawMessage, opts fleet.ApplyTeamSpecOptions) (map[string]uint, error) {
-	verb, path := "POST", "/api/latest/fleet/spec/teams"
+	verb, path := "POST", "/api/latest/fleet/spec/fleets"
 	var responseBody applyTeamSpecsResponse
-	params := map[string]interface{}{"specs": specs}
+	// Rewrite deprecated key names in each team spec to use the new names.
+	rules := endpointer.ExtractAliasRules(fleet.TeamSpec{})
+	rewritten := make([]json.RawMessage, len(specs))
+	for i, spec := range specs {
+		updated, err := endpointer.RewriteOldToNewKeys(spec, rules)
+		if err != nil {
+			return nil, err
+		}
+		rewritten[i] = updated
+	}
+	params := map[string]any{"specs": rewritten}
 	if opts.DryRun && opts.DryRunAssumptions != nil {
 		params["dry_run_assumptions"] = opts.DryRunAssumptions
 	}
@@ -68,7 +79,7 @@ func (c *Client) ApplyTeams(specs []json.RawMessage, opts fleet.ApplyTeamSpecOpt
 
 // PatchFleet sends a partial update to the specified team.
 func (c *Client) PatchFleet(teamID uint, payload fleet.TeamPayload) error {
-	verb, path := "PATCH", "/api/latest/fleet/teams/"+strconv.FormatUint(uint64(teamID), 10)
+	verb, path := "PATCH", "/api/latest/fleet/fleets/"+strconv.FormatUint(uint64(teamID), 10)
 	var resp teamResponse
 	return c.authenticatedRequest(payload, verb, path, &resp)
 }
@@ -81,7 +92,7 @@ func (c *Client) ApplyTeamProfiles(tmName string, profiles []fleet.MDMProfileBat
 	if err != nil {
 		return err
 	}
-	query.Add("team_name", tmName)
+	query.Add("fleet_name", tmName)
 	if opts.DryRunAssumptions != nil && opts.DryRunAssumptions.WindowsEnabledAndConfigured.Valid {
 		query.Add("assume_enabled", strconv.FormatBool(opts.DryRunAssumptions.WindowsEnabledAndConfigured.Value))
 	}
@@ -96,7 +107,7 @@ func (c *Client) ApplyTeamScripts(tmName string, scripts []fleet.ScriptPayload,
 	if err != nil {
 		return nil, err
 	}
-	query.Add("team_name", tmName)
+	query.Add("fleet_name", tmName)
 
 	var resp batchSetScriptsResponse
 	err = c.authenticatedRequestWithQuery(map[string]interface{}{"scripts": scripts}, verb, path, &resp, query.Encode())
@@ -108,7 +119,7 @@ func (c *Client) ApplyTeamSoftwareInstallers(tmName string, softwareInstallers [
 	if err != nil {
 		return nil, err
 	}
-	query.Add("team_name", tmName)
+	query.Add("fleet_name", tmName)
 	return c.applySoftwareInstallers(softwareInstallers, query, opts.DryRun)
 }
 
@@ -117,7 +128,7 @@ func (c *Client) ApplyTeamAppStoreAppsAssociation(tmName string, vppBatchPayload
 	if err != nil {
 		return nil, err
 	}
-	query.Add("team_name", tmName)
+	query.Add("fleet_name", tmName)
 	return c.applyAppStoreAppsAssociation(vppBatchPayload, query)
 }
 
diff --git a/server/service/hosts.go b/server/service/hosts.go
index 12236d2299..b099218368 100644
--- a/server/service/hosts.go
+++ b/server/service/hosts.go
@@ -3232,12 +3232,12 @@ func hostListOptionsFromFilters(filter *map[string]interface{}) (*fleet.HostList
 			} else {
 				return nil, nil, badRequest("label_id must be a number")
 			}
-		case "team_id":
+		case "fleet_id", "team_id":
 			if teamID, ok := v.(float64); ok { // json unmarshals numbers as float64
 				teamID := uint(teamID)
 				opt.TeamFilter = &teamID
 			} else {
-				return nil, nil, badRequest("team_id must be a number")
+				return nil, nil, badRequest("fleet_id must be a number")
 			}
 		case "status":
 			status, ok := v.(string)
diff --git a/server/service/integration_enterprise_test.go b/server/service/integration_enterprise_test.go
index 6de834a163..ef12117d77 100644
--- a/server/service/integration_enterprise_test.go
+++ b/server/service/integration_enterprise_test.go
@@ -12517,7 +12517,7 @@ func (s *integrationEnterpriseTestSuite) TestSoftwareInstallerUploadDownloadAndD
 
 		// check activity
 		s.lastActivityOfTypeMatches(fleet.ActivityTypeDeletedSoftware{}.ActivityName(),
-			fmt.Sprintf(`{"software_title": "ruby", "software_package": "ruby.deb", "software_icon_url": "/api/latest/fleet/software/titles/%d/icon?team_id=0", "team_name": null, "team_id": null, "fleet_name": null, "fleet_id": null, "self_service": true}`, titleID), 0)
+			fmt.Sprintf(`{"software_title": "ruby", "software_package": "ruby.deb", "software_icon_url": "/api/latest/fleet/software/titles/%d/icon?fleet_id=0", "team_name": null, "team_id": null, "fleet_name": null, "fleet_id": null, "self_service": true}`, titleID), 0)
 
 		// download the installer, not found anymore
 		s.Do("GET", fmt.Sprintf("/api/latest/fleet/software/titles/%d/package?alt=media", titleID), nil, http.StatusNotFound, "team_id", fmt.Sprintf("%d", 0))
@@ -13043,7 +13043,7 @@ func (s *integrationEnterpriseTestSuite) TestSoftwareTitleIcons() {
 		headers,
 	)
 	result := parsePutResponse(resp)
-	iconUrl := fmt.Sprintf("/api/latest/fleet/software/titles/%d/icon?team_id=%d", titleID, tm.ID)
+	iconUrl := fmt.Sprintf("/api/latest/fleet/software/titles/%d/icon?fleet_id=%d", titleID, tm.ID)
 	require.Nil(t, result.Err)
 	require.Contains(t, result.IconUrl, iconUrl)
 
diff --git a/server/service/integration_mdm_test.go b/server/service/integration_mdm_test.go
index f3a6ebe660..96124fa2d5 100644
--- a/server/service/integration_mdm_test.go
+++ b/server/service/integration_mdm_test.go
@@ -13841,7 +13841,7 @@ func (s *integrationMDMTestSuite) TestVPPApps() {
 		"team_id",
 		fmt.Sprint(team.ID))
 	s.lastActivityMatches(fleet.ActivityDeletedAppStoreApp{}.ActivityName(),
-		fmt.Sprintf(`{"team_name": "%s", "fleet_name": "%s", "software_title": "%s", "app_store_id": "%s", "software_icon_url": "/api/latest/fleet/software/titles/%d/icon?team_id=%d", "team_id": %d, "fleet_id": %d, "platform": "%s"}`, team.Name, team.Name,
+		fmt.Sprintf(`{"team_name": "%s", "fleet_name": "%s", "software_title": "%s", "app_store_id": "%s", "software_icon_url": "/api/latest/fleet/software/titles/%d/icon?fleet_id=%d", "team_id": %d, "fleet_id": %d, "platform": "%s"}`, team.Name, team.Name,
 			addedApp.Name, addedApp.AdamID, macOSTitleID, team.ID, team.ID, team.ID, addedApp.Platform), 0)
 
 	var count int
@@ -14583,7 +14583,7 @@ func (s *integrationMDMTestSuite) TestNoTeamVPPAppIcons() {
 		"team_id",
 		fmt.Sprint(fleet.PolicyNoTeamID))
 	s.lastActivityMatches(fleet.ActivityDeletedAppStoreApp{}.ActivityName(),
-		fmt.Sprintf(`{"team_name": null, "fleet_name": null, "software_title": "%s", "app_store_id": "%s", "software_icon_url": "/api/latest/fleet/software/titles/%d/icon?team_id=%d", "team_id": %d, "fleet_id": %d, "platform": "%s"}`,
+		fmt.Sprintf(`{"team_name": null, "fleet_name": null, "software_title": "%s", "app_store_id": "%s", "software_icon_url": "/api/latest/fleet/software/titles/%d/icon?fleet_id=%d", "team_id": %d, "fleet_id": %d, "platform": "%s"}`,
 			addedApp.Name, addedApp.AdamID, macOSTitleID, fleet.PolicyNoTeamID, fleet.PolicyNoTeamID, fleet.PolicyNoTeamID, addedApp.Platform), 0)
 
 	mysql.ExecAdhocSQL(t, s.ds, func(q sqlx.ExtContext) error {
diff --git a/server/service/integration_vpp_install_test.go b/server/service/integration_vpp_install_test.go
index 582d621b2a..510773d017 100644
--- a/server/service/integration_vpp_install_test.go
+++ b/server/service/integration_vpp_install_test.go
@@ -1612,7 +1612,7 @@ func (s *integrationMDMTestSuite) TestInHouseAppInstall() {
 			assert.Equal(t, installCmdUUID, cmd.CommandUUID)
 
 			// Points at the expected manifest URL
-			expectedManifestURL := fmt.Sprintf("%s/api/latest/fleet/software/titles/%d/in_house_app/manifest?team_id=%d", s.server.URL, titleID, 0)
+			expectedManifestURL := fmt.Sprintf("%s/api/latest/fleet/software/titles/%d/in_house_app/manifest?fleet_id=%d", s.server.URL, titleID, 0)
 			assert.Contains(t, string(cmd.Raw), expectedManifestURL)
 
 			cmd, err = iosDevice.Acknowledge(cmd.CommandUUID)
@@ -1792,7 +1792,7 @@ func (s *integrationMDMTestSuite) TestInHouseAppSelfInstall() {
 			assert.Equal(t, installCmdUUID, cmd.CommandUUID)
 
 			// Points at the expected manifest URL
-			expectedManifestURL := fmt.Sprintf("%s/api/latest/fleet/software/titles/%d/in_house_app/manifest?team_id=%d", s.server.URL, titleID, 0)
+			expectedManifestURL := fmt.Sprintf("%s/api/latest/fleet/software/titles/%d/in_house_app/manifest?fleet_id=%d", s.server.URL, titleID, 0)
 			assert.Contains(t, string(cmd.Raw), expectedManifestURL)
 
 			cmd, err = iosDevice.Acknowledge(cmd.CommandUUID)
@@ -1891,7 +1891,7 @@ func (s *integrationMDMTestSuite) TestGetInHouseAppManifestUnsignedURL() {
 
 	manifest := readManifest(res)
 	require.NotNil(t, manifest)
-	require.Contains(t, string(manifest), fmt.Sprintf("/%d/in_house_app?team_id=%d", titleID, *teamID))
+	require.Contains(t, string(manifest), fmt.Sprintf("/%d/in_house_app?fleet_id=%d", titleID, *teamID))
 }
 
 func (s *integrationMDMTestSuite) addHostIdentityCertificate(hostUUID string, certSerial uint64) {
diff --git a/server/service/software_title_icons.go b/server/service/software_title_icons.go
index 70a6364669..0c0e5f3734 100644
--- a/server/service/software_title_icons.go
+++ b/server/service/software_title_icons.go
@@ -126,7 +126,12 @@ func (putSoftwareTitleIconRequest) DecodeRequest(ctx context.Context, r *http.Re
 	if titleIDUint64 > math.MaxUint {
 		return nil, &fleet.BadRequestError{Message: "title_id value too large"}
 	}
-	teamID := r.URL.Query().Get("team_id")
+	// Accept both fleet_id and team_id without deprecation warning, since
+	// persisted icon URLs may still contain team_id.
+	teamID := r.URL.Query().Get("fleet_id")
+	if teamID == "" {
+		teamID = r.URL.Query().Get("team_id")
+	}
 	if teamID == "" {
 		return nil, &fleet.BadRequestError{Message: "team_id is required"}
 	}
diff --git a/server/service/transport.go b/server/service/transport.go
index 2fb23ef14f..bbdb67d413 100644
--- a/server/service/transport.go
+++ b/server/service/transport.go
@@ -4,13 +4,16 @@ import (
 	"context"
 	"encoding/json"
 	"fmt"
+	"log/slog"
 	"net/http"
 	"strconv"
 	"strings"
 
 	"github.com/fleetdm/fleet/v4/server/contexts/ctxerr"
+	"github.com/fleetdm/fleet/v4/server/contexts/logging"
 	"github.com/fleetdm/fleet/v4/server/fleet"
 	"github.com/fleetdm/fleet/v4/server/platform/endpointer"
+	platform_logging "github.com/fleetdm/fleet/v4/server/platform/logging"
 	"github.com/fleetdm/fleet/v4/server/ptr"
 	"github.com/gorilla/mux"
 )
@@ -143,7 +146,14 @@ func hostListOptionsFromRequest(r *http.Request) (fleet.HostListOptions, error)
 	teamID := r.URL.Query().Get("fleet_id")
 	if teamID == "" {
 		teamID = r.URL.Query().Get("team_id")
-		// TODO: warn about deprecated team_id parameter if team_id is used instead of fleet_id.
+		if teamID != "" &&
+			platform_logging.TopicEnabled(platform_logging.DeprecatedFieldTopic) {
+			logging.WithLevel(r.Context(), slog.LevelWarn)
+			logging.WithExtras(r.Context(),
+				"deprecated_param", "team_id",
+				"deprecation_warning", "'team_id' is deprecated, use 'fleet_id' instead",
+			)
+		}
 	}
 	if teamID != "" {
 		id, err := strconv.ParseUint(teamID, 10, 32)
@@ -618,8 +628,18 @@ func userListOptionsFromRequest(r *http.Request) (fleet.UserListOptions, error)
 	}
 
 	userOpts := fleet.UserListOptions{ListOptions: opt}
-
-	if tid := r.URL.Query().Get("team_id"); tid != "" {
+	tid := r.URL.Query().Get("fleet_id")
+	if tid == "" {
+		tid = r.URL.Query().Get("team_id")
+		if tid != "" && platform_logging.TopicEnabled(platform_logging.DeprecatedFieldTopic) {
+			logging.WithLevel(r.Context(), slog.LevelWarn)
+			logging.WithExtras(r.Context(),
+				"deprecated_param", "team_id",
+				"deprecation_warning", "'team_id' is deprecated, use 'fleet_id' instead",
+			)
+		}
+	}
+	if tid != "" {
 		teamID, err := strconv.ParseUint(tid, 10, 64)
 		if err != nil {
 			return userOpts, ctxerr.Wrap(r.Context(), badRequest(fmt.Sprintf("Invalid team_id: %s", tid)))
diff --git a/server/worker/jira.go b/server/worker/jira.go
index 5f6d411a16..ce01e9feaa 100644
--- a/server/worker/jira.go
+++ b/server/worker/jira.go
@@ -87,7 +87,7 @@ This issue was created automatically by your Fleet Jira integration.
 * [{{ .DisplayName }}|{{ $.FleetURL }}/hosts/{{ .ID }}]
 {{ end }}
 
-View hosts that failed {{ .PolicyName }} on the [*Hosts*|{{ .FleetURL }}/hosts/manage/?order_key=hostname&order_direction=asc&{{ if .TeamID }}team_id={{ .TeamID }}&{{ end }}policy_id={{ .PolicyID }}&policy_response=failing] page in Fleet.
+View hosts that failed {{ .PolicyName }} on the [*Hosts*|{{ .FleetURL }}/hosts/manage/?order_key=hostname&order_direction=asc&{{ if .TeamID }}fleet_id={{ .TeamID }}&{{ end }}policy_id={{ .PolicyID }}&policy_response=failing] page in Fleet.
 
 ----
 
diff --git a/server/worker/jira_test.go b/server/worker/jira_test.go
index bfe8fa243a..1f3e874f9c 100644
--- a/server/worker/jira_test.go
+++ b/server/worker/jira_test.go
@@ -146,14 +146,14 @@ func TestJiraRun(t *testing.T) {
 			`{"failing_policy":{"policy_id": 1, "policy_name": "test-policy", "hosts": []}}`,
 			`"summary":"test-policy policy failed on 0 host(s)"`,
 			[]string{"\\u0026policy_id=1\\u0026policy_response=failing"},
-			"\\u0026team_id=",
+			"\\u0026fleet_id=",
 		},
 		{
 			"failing team policy",
 			fleet.TierPremium,
 			`{"failing_policy":{"policy_id": 2, "policy_name": "test-policy-2", "team_id": 123, "hosts": [{"id": 1, "hostname": "test-1"}, {"id": 2, "hostname": "test-2"}]}}`,
 			`"summary":"test-policy-2 policy failed on 2 host(s)"`,
-			[]string{"\\u0026team_id=123\\u0026policy_id=2\\u0026policy_response=failing"},
+			[]string{"\\u0026fleet_id=123\\u0026policy_id=2\\u0026policy_response=failing"},
 			"",
 		},
 		{
diff --git a/server/worker/zendesk.go b/server/worker/zendesk.go
index d56fc2751a..f5a7cec7c1 100644
--- a/server/worker/zendesk.go
+++ b/server/worker/zendesk.go
@@ -88,7 +88,7 @@ This ticket was created automatically by your Fleet Zendesk integration.
 * [{{ .DisplayName }}]({{ $.FleetURL }}/hosts/{{ .ID }})
 {{ end }}
 
-View hosts that failed {{ .PolicyName }} on the [**Hosts**]({{ .FleetURL }}/hosts/manage/?order_key=hostname&order_direction=asc&{{ if .TeamID }}team_id={{ .TeamID }}&{{ end }}policy_id={{ .PolicyID }}&policy_response=failing) page in Fleet.
+View hosts that failed {{ .PolicyName }} on the [**Hosts**]({{ .FleetURL }}/hosts/manage/?order_key=hostname&order_direction=asc&{{ if .TeamID }}fleet_id={{ .TeamID }}&{{ end }}policy_id={{ .PolicyID }}&policy_response=failing) page in Fleet.
 
 ----
 
diff --git a/server/worker/zendesk_test.go b/server/worker/zendesk_test.go
index 98a2967ea9..e83ac97e73 100644
--- a/server/worker/zendesk_test.go
+++ b/server/worker/zendesk_test.go
@@ -129,14 +129,14 @@ func TestZendeskRun(t *testing.T) {
 			`{"failing_policy":{"policy_id": 1, "policy_name": "test-policy", "hosts": [{"id": 123, "hostname": "host-123"}]}}`,
 			`"subject":"test-policy policy failed on 1 host(s)"`,
 			[]string{"\\u0026policy_id=1\\u0026policy_response=failing"},
-			"\\u0026team_id=",
+			"\\u0026fleet_id=",
 		},
 		{
 			"failing team policy",
 			fleet.TierPremium,
 			`{"failing_policy":{"policy_id": 2, "policy_name": "test-policy-2", "team_id": 123, "hosts": [{"id": 1, "hostname": "host-1"}, {"id": 2, "hostname": "host-2"}]}}`,
 			`"subject":"test-policy-2 policy failed on 2 host(s)"`,
-			[]string{"\\u0026team_id=123\\u0026policy_id=2\\u0026policy_response=failing"},
+			[]string{"\\u0026fleet_id=123\\u0026policy_id=2\\u0026policy_response=failing"},
 			"",
 		},
 		{