diff --git a/orbit/changes/retry-enroll-on-unauth-error b/orbit/changes/retry-enroll-on-unauth-error
new file mode 100644
index 0000000000..992f59509b
--- /dev/null
+++ b/orbit/changes/retry-enroll-on-unauth-error
@@ -0,0 +1 @@
+* Orbit now re-enroll when encountering a 401/unauthenticated error when communicating with orbit endpoints on Fleet server
diff --git a/orbit/cmd/orbit/orbit.go b/orbit/cmd/orbit/orbit.go
index 3ab2d97444..85d3052fb8 100644
--- a/orbit/cmd/orbit/orbit.go
+++ b/orbit/cmd/orbit/orbit.go
@@ -732,7 +732,7 @@ func getUUID(osqueryPath string) (string, error) {
 // getOrbitNodeKeyOrEnroll attempts to read the orbit node key if the file exists on disk
 // otherwise it enrolls the host with Fleet and saves the node key to disk
 func getOrbitNodeKeyOrEnroll(orbitClient *service.OrbitClient, rootDir string) (string, error) {
-	nodeKeyFilePath := filepath.Join(rootDir, "secret-orbit-node-key.txt")
+	nodeKeyFilePath := filepath.Join(rootDir, constant.OrbitNodeKeyFileName)
 	orbitNodeKey, err := ioutil.ReadFile(nodeKeyFilePath)
 	switch {
 	case err == nil:
@@ -742,20 +742,16 @@ func getOrbitNodeKeyOrEnroll(orbitClient *service.OrbitClient, rootDir string) (
 	default:
 		return "", fmt.Errorf("read orbit node key file: %w", err)
 	}
-	const (
-		orbitEnrollMaxRetries = 10
-		orbitEnrollRetrySleep = 5 * time.Second
-	)
-	for retries := 0; retries < orbitEnrollMaxRetries; retries++ {
+	for retries := 0; retries < constant.OrbitEnrollMaxRetries; retries++ {
 		orbitNodeKey, err := enrollAndWriteNodeKeyFile(orbitClient, nodeKeyFilePath)
 		if err != nil {
 			log.Info().Err(err).Msg("enroll failed, retrying")
-			time.Sleep(orbitEnrollRetrySleep)
+			time.Sleep(constant.OrbitEnrollRetrySleep)
 			continue
 		}
 		return orbitNodeKey, nil
 	}
-	return "", fmt.Errorf("orbit node key enroll failed, attempts=%d", orbitEnrollMaxRetries)
+	return "", fmt.Errorf("orbit node key enroll failed, attempts=%d", constant.OrbitEnrollMaxRetries)
 }
 
 func enrollAndWriteNodeKeyFile(orbitClient *service.OrbitClient, nodeKeyFilePath string) (string, error) {
diff --git a/orbit/pkg/constant/constant.go b/orbit/pkg/constant/constant.go
index c3e6214800..8395e50943 100644
--- a/orbit/pkg/constant/constant.go
+++ b/orbit/pkg/constant/constant.go
@@ -1,5 +1,7 @@
 package constant
 
+import "time"
+
 const (
 	// DefaultDirMode is the default file mode to apply to created directories.
 	DefaultDirMode = 0o755
@@ -12,4 +14,10 @@ const (
 	// We use fleet-desktop as name to properly identify the process when listing
 	// running processes/tasks.
 	DesktopAppExecName = "fleet-desktop"
+	// OrbitNodeKeyFileName is the filename on disk where we write the orbit node key to
+	OrbitNodeKeyFileName = "secret-orbit-node-key.txt"
+	// OrbitEnrollMaxRetries is the max retries when doing an enroll request
+	OrbitEnrollMaxRetries = 10
+	// OrbitEnrollRetrySleep is the time duration to sleep between retries
+	OrbitEnrollRetrySleep = 5 * time.Second
 )
diff --git a/orbit/pkg/update/flag_runner.go b/orbit/pkg/update/flag_runner.go
index 8b02f53ac4..d12bf4615b 100644
--- a/orbit/pkg/update/flag_runner.go
+++ b/orbit/pkg/update/flag_runner.go
@@ -95,6 +95,14 @@ func (r *FlagRunner) DoFlagsUpdate() (bool, error) {
 
 	// next GetConfig from Fleet API
 	flagsJSON, err := r.orbitClient.GetConfig(r.opt.OrbitNodeKey)
+	// on 401 unauthenticated error, re-enroll and update orbit node key
+	if errors.Is(err, service.ErrUnauthenticated) {
+		r.opt.OrbitNodeKey, err = r.updateOrbitNodeKey()
+		if err != nil {
+			return false, err
+		}
+		return false, nil
+	}
 	if err != nil {
 		return false, fmt.Errorf("error getting flags from fleet %w", err)
 	}
@@ -188,3 +196,23 @@ func readFlagFile(rootDir string) (map[string]string, error) {
 	}
 	return result, nil
 }
+
+// updateOrbitNodeKey does re-enrolls by calling the /enroll API and writes the response to disk
+func (r *FlagRunner) updateOrbitNodeKey() (string, error) {
+	for retries := 0; retries < constant.OrbitEnrollMaxRetries; retries++ {
+		newOrbitNodeKey, err := r.orbitClient.DoEnroll()
+		if err != nil {
+			log.Info().Err(err).Msg("re-enroll failed, retrying")
+			time.Sleep(constant.OrbitEnrollRetrySleep)
+			continue
+		}
+		nodeKeyFilePath := filepath.Join(r.opt.RootDir, constant.OrbitNodeKeyFileName)
+		if err := os.WriteFile(nodeKeyFilePath, []byte(newOrbitNodeKey), constant.DefaultFileMode); err != nil {
+			log.Info().Err(err).Msg("failed to write orbit node key to disk")
+			time.Sleep(constant.OrbitEnrollRetrySleep)
+			continue
+		}
+		return newOrbitNodeKey, nil
+	}
+	return "", fmt.Errorf("orbit re-enroll failed, attempts=%d", constant.OrbitEnrollMaxRetries)
+}