diff --git a/cmd/headscale/cli/root.go b/cmd/headscale/cli/root.go
index 7f84fb8a..69c135e3 100644
--- a/cmd/headscale/cli/root.go
+++ b/cmd/headscale/cli/root.go
@@ -1,7 +1,6 @@
 package cli
 
 import (
-	"fmt"
 	"os"
 	"runtime"
 	"slices"
@@ -39,6 +38,14 @@ func init() {
 		StringP("output", "o", "", "Output format. Empty for human-readable, 'json', 'json-line' or 'yaml'")
 	rootCmd.PersistentFlags().
 		Bool("force", false, "Disable prompts and forces the execution")
+
+	// Re-enable usage output only for flag-parsing errors; runtime errors
+	// from RunE should never dump usage text.
+	rootCmd.SetFlagErrorFunc(func(cmd *cobra.Command, err error) error {
+		cmd.SilenceUsage = false
+
+		return err
+	})
 }
 
 func initConfig() {
@@ -140,12 +147,15 @@ var rootCmd = &cobra.Command{
 headscale is an open source implementation of the Tailscale control server
 
 https://github.com/juanfont/headscale`,
+	SilenceErrors: true,
+	SilenceUsage:  true,
 }
 
 func Execute() {
-	err := rootCmd.Execute()
+	cmd, err := rootCmd.ExecuteC()
 	if err != nil {
-		fmt.Fprintln(os.Stderr, err)
+		outputFormat, _ := cmd.Flags().GetString("output")
+		printError(err, outputFormat)
 		os.Exit(1)
 	}
 }
diff --git a/cmd/headscale/cli/utils.go b/cmd/headscale/cli/utils.go
index 31087569..eef83cc0 100644
--- a/cmd/headscale/cli/utils.go
+++ b/cmd/headscale/cli/utils.go
@@ -203,6 +203,34 @@ func ErrorOutput(errResult error, override string, outputFormat string) {
 	os.Exit(1)
 }
 
+// printError writes err to stderr, formatting it as JSON/YAML when the
+// --output flag requests machine-readable output.  Used exclusively by
+// Execute() so that every error surfaces in the format the caller asked for.
+func printError(err error, outputFormat string) {
+	type errOutput struct {
+		Error string `json:"error"`
+	}
+
+	e := errOutput{Error: err.Error()}
+
+	var formatted []byte
+
+	switch outputFormat {
+	case "json":
+		formatted, _ = json.MarshalIndent(e, "", "\t") //nolint:errchkjson // errOutput contains only a string field
+	case "json-line":
+		formatted, _ = json.Marshal(e) //nolint:errchkjson // errOutput contains only a string field
+	case "yaml":
+		formatted, _ = yaml.Marshal(e)
+	default:
+		fmt.Fprintf(os.Stderr, "Error: %s\n", err)
+
+		return
+	}
+
+	fmt.Fprintf(os.Stderr, "%s\n", formatted)
+}
+
 func HasMachineOutputFlag() bool {
 	for _, arg := range os.Args {
 		if arg == "json" || arg == "json-line" || arg == "yaml" {