diff --git a/.github/workflows/generate-desktop-targets.yml b/.github/workflows/generate-desktop-targets.yml
index 4233c7291f..d3854175ef 100644
--- a/.github/workflows/generate-desktop-targets.yml
+++ b/.github/workflows/generate-desktop-targets.yml
@@ -63,7 +63,7 @@ jobs:
           path: desktop.app.tar.gz
 
   desktop-windows:
-    runs-on: macos-latest
+    runs-on: ubuntu-latest
     steps:
 
       - name: Install Go
@@ -83,4 +83,27 @@ jobs:
         uses: actions/upload-artifact@6673cd052c4cd6fcf4b4e6e60ea986c889389535 # v2
         with:
           name: fleet-desktop.exe
-          path: fleet-desktop.exe
\ No newline at end of file
+          path: fleet-desktop.exe
+
+  desktop-linux:
+    runs-on: ubuntu-latest
+    steps:
+
+      - name: Install Go
+        uses: actions/setup-go@f6164bd8c8acb4a71fb2791a8b6c4024ff038dab # v2
+        with:
+          go-version: '^1.17.0'
+
+      - name: Checkout
+        uses: actions/checkout@629c2de402a417ea7690ca6ce3f33229e27606a5 # v2
+
+      - name: Generate desktop.tar.gz
+        run: |
+          FLEET_DESKTOP_VERSION=$FLEET_DESKTOP_VERSION \
+          make desktop-linux
+
+      - name: Upload desktop.tar.gz
+        uses: actions/upload-artifact@6673cd052c4cd6fcf4b4e6e60ea986c889389535 # v2
+        with:
+          name: desktop.tar.gz
+          path: desktop.tar.gz
\ No newline at end of file
diff --git a/.gitignore b/.gitignore
index e1a87bf011..57e5768caf 100644
--- a/.gitignore
+++ b/.gitignore
@@ -60,6 +60,7 @@ terraform.tfstate*
 # generated installers
 fleet-osquery*
 desktop.app.tar.gz
+desktop.tar.gz
 
 # residual files when running the cpe command
 cmd/cpe/etagenv
diff --git a/Dockerfile-desktop-linux b/Dockerfile-desktop-linux
new file mode 100644
index 0000000000..be2ffd4b9a
--- /dev/null
+++ b/Dockerfile-desktop-linux
@@ -0,0 +1,19 @@
+FROM golang:1.17.8-bullseye
+LABEL maintainer="Fleet Developers <hello@fleetdm.com>"
+
+RUN apt-get update && apt-get install -y \
+	gcc \
+	libgtk-3-dev \
+	libayatana-appindicator3-dev \
+	&& rm -rf /var/lib/apt/lists/*
+
+RUN mkdir -p /usr/src/fleet
+RUN mkdir -p /output
+
+WORKDIR /usr/src/fleet
+
+COPY orbit ./orbit
+COPY pkg ./pkg
+COPY go.mod go.sum ./
+
+CMD /bin/bash
diff --git a/Makefile b/Makefile
index 620cfb1d91..a29c17335e 100644
--- a/Makefile
+++ b/Makefile
@@ -175,6 +175,10 @@ deps-js:
 
 deps-go:
 	go mod download
+ifeq ($(shell uname -s),Linux)
+	# Dependency required for Linux Fleet Desktop.
+	sudo apt-get install gcc libgtk-3-dev libayatana-appindicator3-dev -y
+endif
 
 migration:
 	go run github.com/fleetdm/goose/cmd/goose -dir server/datastore/mysql/migrations/tables create $(name)
@@ -306,6 +310,8 @@ endif
 #
 # Usage:
 # FLEET_DESKTOP_APPLE_AUTHORITY=foo FLEET_DESKTOP_VERSION=0.0.1 make desktop-app-tar-gz
+#
+# Output: desktop.app.tar.gz
 desktop-app-tar-gz:
 ifneq ($(shell uname), Darwin)
 	@echo "Makefile target desktop-app-tar-gz is only supported on macOS"
@@ -313,12 +319,37 @@ ifneq ($(shell uname), Darwin)
 endif
 	go run ./tools/desktop macos
 
+FLEET_DESKTOP_VERSION ?= unknown
+
 # Build desktop executable for Windows.
 #
 # Usage:
 # FLEET_DESKTOP_VERSION=0.0.1 make desktop-windows
+#
+# Output: fleet-desktop.exe
 desktop-windows:
-	GOOS=windows GOARCH=amd64 go build -ldflags "-H=windowsgui" -o fleet-desktop.exe ./orbit/cmd/desktop
+	GOOS=windows GOARCH=amd64 go build -ldflags "-H=windowsgui -X=main.version=$(FLEET_DESKTOP_VERSION)" -o fleet-desktop.exe ./orbit/cmd/desktop
+
+# Build desktop executable for Linux.
+#
+# Usage:
+# FLEET_DESKTOP_VERSION=0.0.1 make desktop-linux
+#
+# Output: desktop.tar.gz
+desktop-linux:
+	docker build -f Dockerfile-desktop-linux -t desktop-linux-builder .
+	docker run --rm -v $(shell pwd):/output desktop-linux-builder /bin/bash -c "\
+		mkdir /output/fleet-desktop && \
+		go build -o /output/fleet-desktop/fleet-desktop -ldflags "-X=main.version=$(FLEET_DESKTOP_VERSION)" /usr/src/fleet/orbit/cmd/desktop && \
+		cp /usr/lib/x86_64-linux-gnu/libayatana-appindicator3.so.1 \
+		/usr/lib/x86_64-linux-gnu/libayatana-ido3-0.4.so.0 \
+		/usr/lib/x86_64-linux-gnu/libayatana-indicator3.so.7 \
+		/lib/x86_64-linux-gnu/libm.so.6 \
+		/usr/lib/x86_64-linux-gnu/libdbusmenu-gtk3.so.4 \
+		/usr/lib/x86_64-linux-gnu/libdbusmenu-glib.so.4 \
+		/output/fleet-desktop && cd /output && \
+		tar czf desktop.tar.gz fleet-desktop && \
+		rm -r fleet-desktop"
 
 # db-replica-setup setups one main and one read replica MySQL instance for dev/testing.
 #	- Assumes the docker containers are already running (tools/mysql-replica-testing/docker-compose.yml)
diff --git a/changes/issue-4925-fleet-desktop-linux b/changes/issue-4925-fleet-desktop-linux
new file mode 100644
index 0000000000..04ed91f9d8
--- /dev/null
+++ b/changes/issue-4925-fleet-desktop-linux
@@ -0,0 +1 @@
+* Add (beta) support for Fleet Desktop to linux.
diff --git a/ee/fleetctl/updates.go b/ee/fleetctl/updates.go
index 3efc8d1a06..7c2d7d08b1 100644
--- a/ee/fleetctl/updates.go
+++ b/ee/fleetctl/updates.go
@@ -251,6 +251,9 @@ func updatesAddFunc(c *cli.Context) error {
 		case name == "desktop" && platform == "windows":
 			// This is a special case for the desktop target on Windows.
 			dstPath = filepath.Join(filepath.Dir(dstPath), constant.DesktopAppExecName+".exe")
+		case name == "desktop" && platform == "linux":
+			// This is a special case for the desktop target on Linux.
+			dstPath += ".tar.gz"
 		case strings.HasSuffix(target, ".exe"):
 			dstPath += ".exe"
 		case strings.HasSuffix(target, ".app.tar.gz"):
diff --git a/orbit/cmd/desktop/desktop.go b/orbit/cmd/desktop/desktop.go
index f20a4e46f6..0b7884088d 100644
--- a/orbit/cmd/desktop/desktop.go
+++ b/orbit/cmd/desktop/desktop.go
@@ -1,6 +1,3 @@
-//go:build darwin || windows
-// +build darwin windows
-
 package main
 
 import (
@@ -17,12 +14,15 @@ import (
 	"github.com/getlantern/systray"
 )
 
+var version = "unknown"
+
 func main() {
 	// Our TUF provided targets must support launching with "--help".
 	if len(os.Args) > 1 && os.Args[1] == "--help" {
 		fmt.Println("Fleet Desktop application executable")
 		return
 	}
+	log.Printf("fleet-desktop version=%s\n", version)
 
 	devURL := os.Getenv("FLEET_DESKTOP_DEVICE_URL")
 	if devURL == "" {
diff --git a/orbit/cmd/desktop/desktop_unix.go b/orbit/cmd/desktop/desktop_unix.go
index 5fe818a7ab..45bcc0dbdb 100644
--- a/orbit/cmd/desktop/desktop_unix.go
+++ b/orbit/cmd/desktop/desktop_unix.go
@@ -1,7 +1,5 @@
-//go:build darwin
-// +build darwin
-
-// TODO(lucas): Once we support Linux, amend the above build tags.
+//go:build darwin || linux
+// +build darwin linux
 
 package main
 
diff --git a/orbit/cmd/orbit/orbit.go b/orbit/cmd/orbit/orbit.go
index 562c370f2b..8ba56e42d0 100644
--- a/orbit/cmd/orbit/orbit.go
+++ b/orbit/cmd/orbit/orbit.go
@@ -229,6 +229,8 @@ func main() {
 				opt.Targets["desktop"] = update.DesktopMacOSTarget
 			case "windows":
 				opt.Targets["desktop"] = update.DesktopWindowsTarget
+			case "linux":
+				opt.Targets["desktop"] = update.DesktopLinuxTarget
 			default:
 				log.Fatal().Str("GOOS", runtime.GOOS).Msg("unsupported GOOS for desktop target")
 			}
@@ -321,7 +323,7 @@ func main() {
 
 		if !c.Bool("disable-updates") {
 			targets := []string{"orbit", "osqueryd"}
-			if c.Bool("fleet-desktop") && (runtime.GOOS == "darwin" || runtime.GOOS == "windows") {
+			if c.Bool("fleet-desktop") {
 				targets = append(targets, "desktop")
 			}
 			updateRunner, err := update.NewRunner(updater, update.RunnerOptions{
@@ -483,7 +485,7 @@ func main() {
 		}))
 		g.Add(ext.Execute, ext.Interrupt)
 
-		if c.Bool("fleet-desktop") && (runtime.GOOS == "darwin" || runtime.GOOS == "windows") {
+		if c.Bool("fleet-desktop") {
 			desktopRunner := newDesktopRunner(desktopPath, fleetURL, deviceAuthToken, c.Bool("insecure"))
 			g.Add(desktopRunner.actor())
 		}
@@ -557,7 +559,7 @@ func (d *desktopRunner) execute() error {
 
 	for {
 		// First retry logic to start fleet-desktop.
-		if done := retry(30*time.Second, d.interruptCh, func() bool {
+		if done := retry(30*time.Second, false, d.interruptCh, func() bool {
 			// Orbit runs as root user on Unix and as SYSTEM (Windows Service) user on Windows.
 			// To be able to run the desktop application (mostly to register the icon in the system tray)
 			// we need to run the application as the login user.
@@ -572,7 +574,8 @@ func (d *desktopRunner) execute() error {
 		}
 
 		// Second retry logic to monitor fleet-desktop.
-		if done := retry(30*time.Second, d.interruptCh, func() bool {
+		// Call with waitFirst=true to give some time for the process to start.
+		if done := retry(30*time.Second, true, d.interruptCh, func() bool {
 			switch _, err := getProcessByName(constant.DesktopAppExecName); {
 			case err == nil:
 				return true // all good, process is running, retry.
@@ -589,14 +592,17 @@ func (d *desktopRunner) execute() error {
 	}
 }
 
-func retry(d time.Duration, done chan struct{}, fn func() bool) bool {
+func retry(d time.Duration, waitFirst bool, done chan struct{}, fn func() bool) bool {
 	ticker := time.NewTicker(d)
 	defer ticker.Stop()
 
 	for {
-		if retry := fn(); !retry {
-			return false
+		if !waitFirst {
+			if retry := fn(); !retry {
+				return false
+			}
 		}
+		waitFirst = false
 		select {
 		case <-done:
 			return true
diff --git a/orbit/pkg/execuser/execuser_linux.go b/orbit/pkg/execuser/execuser_linux.go
index 77fe5aa6a9..df245b40b6 100644
--- a/orbit/pkg/execuser/execuser_linux.go
+++ b/orbit/pkg/execuser/execuser_linux.go
@@ -1,5 +1,114 @@
 package execuser
 
+import (
+	"fmt"
+	"os"
+	"os/exec"
+	"path/filepath"
+	"strconv"
+	"strings"
+
+	"github.com/rs/zerolog/log"
+)
+
+// run uses sudo to run the given path as login user.
 func run(path string, opts eopts) error {
-	panic("unimplemented")
+	user, err := getLoginUID()
+	if err != nil {
+		return fmt.Errorf("get user: %w", err)
+	}
+
+	log.Info().
+		Str("user", user.name).
+		Int64("id", user.id).
+		Msg("running sudo")
+
+	arg := []string{"-u", user.name, "-H"}
+	for _, nv := range opts.env {
+		arg = append(arg, fmt.Sprintf("%s=%s", nv[0], nv[1]))
+	}
+	arg = append(arg,
+		// TODO(lucas): Default to display 0, revisit when working on
+		// multi-user/multi-session support. This assumes there's only
+		// one desktop session and belongs to the user returned in `getLoginUID'.
+		"DISPLAY=:0",
+		// DBUS_SESSION_BUS_ADDRESS sets the location of the user login session bus.
+		// Required by the libayatana-appindicator3 library to display a tray icon
+		// on the desktop session.
+		fmt.Sprintf("DBUS_SESSION_BUS_ADDRESS=unix:path=/run/user/%d/bus", user.id),
+		fmt.Sprintf("LD_LIBRARY_PATH=%s:%s", filepath.Dir(path), os.ExpandEnv("$LD_LIBRARY_PATH")),
+		path,
+	)
+
+	cmd := exec.Command("sudo", arg...)
+	cmd.Stderr = os.Stderr
+	cmd.Stdout = os.Stdout
+	log.Printf("cmd=%s", cmd.String())
+
+	if err := cmd.Start(); err != nil {
+		return fmt.Errorf("open path %q: %w", path, err)
+	}
+	return nil
+}
+
+type user struct {
+	name string
+	id   int64
+}
+
+// getLoginUID returns the name and uid of the first login user
+// as reported by the `users' command.
+//
+// NOTE(lucas): It is always picking first login user as returned
+// by `users', revisit when working on multi-user/multi-session support.
+func getLoginUID() (*user, error) {
+	out, err := exec.Command("users").CombinedOutput()
+	if err != nil {
+		return nil, fmt.Errorf("users exec failed: %w", err)
+	}
+	usernames := parseUsersOutput(string(out))
+	username := usernames[0]
+	if username == "" {
+		return nil, fmt.Errorf("no user session found")
+	}
+	out, err = exec.Command("id", "-u", username).CombinedOutput()
+	if err != nil {
+		return nil, fmt.Errorf("id exec failed: %w", err)
+	}
+	uid, err := parseIDOutput(string(out))
+	if err != nil {
+		return nil, err
+	}
+	return &user{
+		name: username,
+		id:   uid,
+	}, nil
+}
+
+// parseUsersOutput parses the output of the `users' command.
+//
+// 	`users' command prints on a single line a blank-separated list of user names of
+// 	users currently logged in to the current host. Each user name
+// 	corresponds to a login session, so if a user has more than one login
+// 	session, that user's name will appear the same number of times in the
+// 	output.
+//
+// Returns the list of usernames.
+func parseUsersOutput(s string) []string {
+	var users []string
+	for _, userCol := range strings.Split(strings.TrimSpace(s), " ") {
+		users = append(users, userCol)
+	}
+	return users
+}
+
+// parseIDOutput parses the output of the `id' command.
+//
+// Returns the parsed uid.
+func parseIDOutput(s string) (int64, error) {
+	uid, err := strconv.ParseInt(strings.TrimSpace(string(s)), 10, 0)
+	if err != nil {
+		return 0, fmt.Errorf("failed to parse uid: %w", err)
+	}
+	return uid, nil
 }
diff --git a/orbit/pkg/packaging/linux_shared.go b/orbit/pkg/packaging/linux_shared.go
index 76579b9946..1d25047161 100644
--- a/orbit/pkg/packaging/linux_shared.go
+++ b/orbit/pkg/packaging/linux_shared.go
@@ -40,6 +40,12 @@ func buildNFPM(opt Options, pkger nfpm.Packager) (string, error) {
 	updateOpt.RootDirectory = orbitRoot
 	updateOpt.Targets = update.LinuxTargets
 
+	if opt.Desktop {
+		updateOpt.Targets["desktop"] = update.DesktopLinuxTarget
+		// Override default channel with the provided value.
+		updateOpt.Targets.SetTargetChannel("desktop", opt.DesktopChannel)
+	}
+
 	// Override default channels with the provided values.
 	updateOpt.Targets.SetTargetChannel("orbit", opt.OrbitChannel)
 	updateOpt.Targets.SetTargetChannel("osqueryd", opt.OsquerydChannel)
@@ -235,6 +241,10 @@ ORBIT_UPDATE_URL={{ .UpdateURL }}
 ORBIT_ORBIT_CHANNEL={{ .OrbitChannel }}
 ORBIT_OSQUERYD_CHANNEL={{ .OsquerydChannel }}
 ORBIT_UPDATE_INTERVAL={{ .OrbitUpdateInterval }}
+{{ if .Desktop }}
+ORBIT_FLEET_DESKTOP=true
+ORBIT_DESKTOP_CHANNEL={{ .DesktopChannel }}
+{{ end }}
 {{ if .Insecure }}ORBIT_INSECURE=true{{ end }}
 {{ if .DisableUpdates }}ORBIT_DISABLE_UPDATES=true{{ end }}
 {{ if .FleetURL }}ORBIT_FLEET_URL={{.FleetURL}}{{ end }}
@@ -295,12 +305,13 @@ func writePostInstall(opt Options, path string) error {
 }
 
 func writePreRemove(opt Options, path string) error {
+	// We add `|| true` in case the service is not running
+	// or has been manually disabled already. Otherwise,
+	// uninstallation fails.
 	if err := ioutil.WriteFile(path, []byte(`#!/bin/sh
 
-set -e
-
-systemctl stop orbit.service
-systemctl disable orbit.service
+systemctl stop orbit.service || true
+systemctl disable orbit.service || true
 `), constant.DefaultFileMode); err != nil {
 		return fmt.Errorf("write file: %w", err)
 	}
diff --git a/orbit/pkg/update/options.go b/orbit/pkg/update/options.go
index 4d716ed367..73b8252e81 100644
--- a/orbit/pkg/update/options.go
+++ b/orbit/pkg/update/options.go
@@ -1,6 +1,13 @@
 package update
 
-import "github.com/fleetdm/fleet/v4/orbit/pkg/constant"
+import (
+	"fmt"
+	"os"
+	"os/exec"
+	"path/filepath"
+
+	"github.com/fleetdm/fleet/v4/orbit/pkg/constant"
+)
 
 // DefaultOptions are the default options to use when creating an update
 // client.
@@ -59,4 +66,19 @@ var (
 		Channel:    "stable",
 		TargetFile: constant.DesktopAppExecName + ".exe",
 	}
+
+	DesktopLinuxTarget = TargetInfo{
+		Platform:             "linux",
+		Channel:              "stable",
+		TargetFile:           "desktop.tar.gz",
+		ExtractedExecSubPath: []string{"fleet-desktop", constant.DesktopAppExecName},
+		CustomCheckExec: func(execPath string) error {
+			cmd := exec.Command(execPath, "--help")
+			cmd.Env = append(cmd.Env, fmt.Sprintf("LD_LIBRARY_PATH=%s:%s", filepath.Dir(execPath), os.ExpandEnv("$LD_LIBRARY_PATH")))
+			if out, err := cmd.CombinedOutput(); err != nil {
+				return fmt.Errorf("exec new version: %s: %w", string(out), err)
+			}
+			return nil
+		},
+	}
 )
diff --git a/orbit/pkg/update/update.go b/orbit/pkg/update/update.go
index 2f31c7de45..113d0f7f2c 100644
--- a/orbit/pkg/update/update.go
+++ b/orbit/pkg/update/update.go
@@ -85,6 +85,8 @@ type TargetInfo struct {
 	// ExtractedExecSubPath is the path to the executable in case the
 	// target is a compressed file.
 	ExtractedExecSubPath []string
+	// CustomCheckExec allows for a custom method for checking a downloaded executable.
+	CustomCheckExec func(execPath string) error
 }
 
 // New creates a new updater given the provided options. All the necessary
@@ -286,7 +288,7 @@ func (u *Updater) Get(target string) (*LocalTarget, error) {
 		}
 		if err := checkFileHash(meta, localTarget.Path); err != nil {
 			log.Debug().Str("info", err.Error()).Msg("change detected")
-			if err := u.download(target, repoPath, localTarget.Path); err != nil {
+			if err := u.download(target, repoPath, localTarget.Path, localTarget.Info.CustomCheckExec); err != nil {
 				return nil, fmt.Errorf("download %q: %w", repoPath, err)
 			}
 			if strings.HasSuffix(localTarget.Path, ".tar.gz") {
@@ -299,7 +301,7 @@ func (u *Updater) Get(target string) (*LocalTarget, error) {
 		}
 	case errors.Is(err, os.ErrNotExist):
 		log.Debug().Err(err).Msg("stat file")
-		if err := u.download(target, repoPath, localTarget.Path); err != nil {
+		if err := u.download(target, repoPath, localTarget.Path, localTarget.Info.CustomCheckExec); err != nil {
 			return nil, fmt.Errorf("download %q: %w", repoPath, err)
 		}
 	default:
@@ -375,7 +377,7 @@ func (u *Updater) CopyDevBuild(target, devBuildPath string) {
 
 // download downloads the target to the provided path. The file is deleted and
 // an error is returned if the hash does not match.
-func (u *Updater) download(target, repoPath, localPath string) error {
+func (u *Updater) download(target, repoPath, localPath string, customCheckExec func(execPath string) error) error {
 	staging := filepath.Join(u.opt.RootDirectory, stagingDir)
 
 	if err := secure.MkdirAll(staging, constant.DefaultDirMode); err != nil {
@@ -422,7 +424,7 @@ func (u *Updater) download(target, repoPath, localPath string) error {
 		return fmt.Errorf("close tmp file: %w", err)
 	}
 
-	if err := u.checkExec(target, tmp.Name()); err != nil {
+	if err := u.checkExec(target, tmp.Name(), customCheckExec); err != nil {
 		return fmt.Errorf("exec check failed %q: %w", tmp.Name(), err)
 	}
 
@@ -452,7 +454,7 @@ func goosFromPlatform(platform string) (string, error) {
 }
 
 // checkExec checks/verifies a downloaded executable target by executing it.
-func (u *Updater) checkExec(target, tmpPath string) error {
+func (u *Updater) checkExec(target, tmpPath string, customCheckExec func(execPath string) error) error {
 	localTarget, err := u.localTarget(target)
 	if err != nil {
 		return err
@@ -477,11 +479,18 @@ func (u *Updater) checkExec(target, tmpPath string) error {
 		tmpPath = filepath.Join(append([]string{filepath.Dir(tmpPath)}, localTarget.Info.ExtractedExecSubPath...)...)
 	}
 
-	// Note that this would fail for any binary that returns nonzero for --help.
-	out, err := exec.Command(tmpPath, "--help").CombinedOutput()
-	if err != nil {
-		return fmt.Errorf("exec new version: %s: %w", string(out), err)
+	if customCheckExec != nil {
+		if err := customCheckExec(tmpPath); err != nil {
+			return fmt.Errorf("custom exec new version failed: %w", err)
+		}
+	} else {
+		// Note that this would fail for any binary that returns nonzero for --help.
+		cmd := exec.Command(tmpPath, "--help")
+		if out, err := cmd.CombinedOutput(); err != nil {
+			return fmt.Errorf("exec new version: %s: %w", string(out), err)
+		}
 	}
+
 	return nil
 }
 
diff --git a/tools/desktop/desktop.go b/tools/desktop/desktop.go
index cbbe22bc12..7109f62b6a 100644
--- a/tools/desktop/desktop.go
+++ b/tools/desktop/desktop.go
@@ -147,7 +147,11 @@ func createMacOSApp(version, authority string, notarize bool) error {
 	}
 
 	/* #nosec G204 -- arguments are actually well defined */
-	buildExec := exec.Command("go", "build", "-o", filepath.Join(macOSDir, constant.DesktopAppExecName), "./"+filepath.Join("orbit", "cmd", "desktop"))
+	buildExec := exec.Command("go", "build",
+		"-o", filepath.Join(macOSDir, constant.DesktopAppExecName),
+		"-ldflags", os.ExpandEnv("-X=main.version=$FLEET_DESKTOP_VERSION"),
+		"./"+filepath.Join("orbit", "cmd", "desktop"),
+	)
 	buildExec.Env = append(os.Environ(), "CGO_ENABLED=1")
 	buildExec.Stderr = os.Stderr
 	buildExec.Stdout = os.Stdout
diff --git a/tools/tuf/init_tuf.sh b/tools/tuf/init_tuf.sh
index 75e412d1c9..5f8cb538a8 100755
--- a/tools/tuf/init_tuf.sh
+++ b/tools/tuf/init_tuf.sh
@@ -89,6 +89,19 @@ function create_repository() {
       rm fleet-desktop.exe
     fi
 
+    # Add Fleet Desktop application on  (if enabled).
+    if [[ $system == "linux" && -n "$FLEET_DESKTOP" ]]; then
+      FLEET_DESKTOP_VERSION=42.0.0 \
+      make desktop-linux
+      ./build/fleetctl updates add \
+        --path $TUF_PATH \
+        --target desktop.tar.gz \
+        --platform linux \
+        --name desktop \
+        --version 42.0.0 -t 42.0 -t 42 -t stable
+      rm desktop.tar.gz
+    fi
+
   done
 
   # Generate and add osqueryd .app bundle for macos-app.
@@ -146,6 +159,7 @@ if [ -n "$GENERATE_PKGS" ]; then
   echo "Generating deb..."
   ./build/fleetctl package \
     --type=deb \
+    ${FLEET_DESKTOP:+--fleet-desktop} \
     --fleet-url=https://$DEB_HOSTNAME:8080 \
     --enroll-secret=$ENROLL_SECRET \
     --insecure \
@@ -158,6 +172,7 @@ if [ -n "$GENERATE_PKGS" ]; then
   echo "Generating rpm..."
   ./build/fleetctl package \
     --type=rpm \
+    ${FLEET_DESKTOP:+--fleet-desktop} \
     --fleet-url=https://$RPM_HOSTNAME:8080 \
     --enroll-secret=$ENROLL_SECRET \
     --insecure \