diff --git a/changes/43721-clean-up-gitops-errors b/changes/43721-clean-up-gitops-errors
new file mode 100644
index 0000000000..f989896ecc
--- /dev/null
+++ b/changes/43721-clean-up-gitops-errors
@@ -0,0 +1 @@
+- Improved errors returned from API when running fleetctl commands by dropping path / status code.
diff --git a/cmd/fleetctl/fleetctl/clean_error.go b/cmd/fleetctl/fleetctl/clean_error.go
new file mode 100644
index 0000000000..654c95c4d0
--- /dev/null
+++ b/cmd/fleetctl/fleetctl/clean_error.go
@@ -0,0 +1,38 @@
+package fleetctl
+
+import (
+	"errors"
+	"regexp"
+
+	"github.com/fleetdm/fleet/v4/client"
+)
+
+// statusCodeErrPrefixRE matches the "<VERB> <path> received status <code> "
+// prefix that BaseClient.ParseResponse adds when wrapping a *StatusCodeErr.
+// VERB is uppercase (GET, POST, PATCH, ...) and path starts with "/".
+var statusCodeErrPrefixRE = regexp.MustCompile(`[A-Z]+ /\S* received status \d+ `)
+
+// CleanStatusCodeErr returns a copy of err suitable for display in fleetctl
+// CLI output. If the chain contains a *client.StatusCodeErr, the verbose
+// "VERB /path received status N " prefix added by the HTTP client is stripped
+// so users see only the server-provided reason. If no StatusCodeErr is in the
+// chain, err is returned unchanged.
+//
+// The returned value is for printing only — it does not preserve the original
+// error chain, so callers that need to inspect err with errors.Is / errors.As
+// should do so against the original error before passing it here.
+func CleanStatusCodeErr(err error) error {
+	if err == nil {
+		return nil
+	}
+	var sce *client.StatusCodeErr
+	if !errors.As(err, &sce) {
+		return err
+	}
+	// Strip the first instance of the status code error prefix from the message, if present.
+	msg := err.Error()
+	if loc := statusCodeErrPrefixRE.FindStringIndex(msg); loc != nil {
+		msg = msg[:loc[0]] + msg[loc[1]:]
+	}
+	return errors.New(msg)
+}
diff --git a/cmd/fleetctl/fleetctl/clean_error_test.go b/cmd/fleetctl/fleetctl/clean_error_test.go
new file mode 100644
index 0000000000..42542d3763
--- /dev/null
+++ b/cmd/fleetctl/fleetctl/clean_error_test.go
@@ -0,0 +1,37 @@
+package fleetctl
+
+import (
+	"errors"
+	"fmt"
+	"testing"
+
+	"github.com/fleetdm/fleet/v4/client"
+	"github.com/stretchr/testify/require"
+)
+
+func TestCleanStatusCodeErr(t *testing.T) {
+	sce := &client.StatusCodeErr{Code: 422, Body: "Validation Failed: name may not be empty"}
+	wrapped := fmt.Errorf("PATCH /api/latest/fleet/config received status %w", sce)
+	outer := fmt.Errorf("applying fleet config: %w", wrapped)
+
+	cases := []struct {
+		name string
+		in   error
+		want string
+	}{
+		{"nil", nil, ""},
+		{"plain error untouched", errors.New("boom"), "boom"},
+		{"bare wrapped status code err", wrapped, "Validation Failed: name may not be empty"},
+		{"outer-wrapped status code err", outer, "applying fleet config: Validation Failed: name may not be empty"},
+	}
+	for _, tc := range cases {
+		t.Run(tc.name, func(t *testing.T) {
+			got := CleanStatusCodeErr(tc.in)
+			if tc.in == nil {
+				require.NoError(t, got)
+				return
+			}
+			require.Equal(t, tc.want, got.Error())
+		})
+	}
+}
diff --git a/cmd/fleetctl/main.go b/cmd/fleetctl/main.go
index e2d1f1d398..2e47be997d 100644
--- a/cmd/fleetctl/main.go
+++ b/cmd/fleetctl/main.go
@@ -23,7 +23,7 @@ func main() {
 	app := fleetctl.CreateApp(os.Stdin, os.Stdout, os.Stderr, exitErrHandler)
 	fleetctl.StashRawArgs(app, os.Args)
 	if err := app.Run(os.Args); err != nil {
-		fmt.Fprintf(os.Stdout, "Error: %+v\n", err)
+		fmt.Fprintf(os.Stdout, "Error: %+v\n", fleetctl.CleanStatusCodeErr(err))
 		os.Exit(1)
 	}
 }
@@ -34,7 +34,7 @@ func exitErrHandler(c *cli.Context, err error) {
 		return
 	}
 
-	fmt.Fprintf(c.App.ErrWriter, "Error: %+v\n", err)
+	fmt.Fprintf(c.App.ErrWriter, "Error: %+v\n", fleetctl.CleanStatusCodeErr(err))
 
 	if errors.Is(err, fs.ErrPermission) {
 		switch runtime.GOOS {