diff --git a/clientupdate/clientupdate.go b/clientupdate/clientupdate.go
index 2bfb0f294..f3b8dca7c 100644
--- a/clientupdate/clientupdate.go
+++ b/clientupdate/clientupdate.go
@@ -29,6 +29,7 @@
 
 	"github.com/google/uuid"
 	"tailscale.com/clientupdate/distsign"
+	"tailscale.com/hostinfo"
 	"tailscale.com/types/logger"
 	"tailscale.com/util/cmpver"
 	"tailscale.com/util/winutil"
@@ -162,9 +163,10 @@ func NewUpdater(args Arguments) (*Updater, error) {
 type updateFunction func() error
 
 func (up *Updater) getUpdateFunction() (fn updateFunction, canAutoUpdate bool) {
+	canAutoUpdate = !hostinfo.New().Container.EqualBool(true) // EqualBool(false) would return false if the value is not set.
 	switch runtime.GOOS {
 	case "windows":
-		return up.updateWindows, true
+		return up.updateWindows, canAutoUpdate
 	case "linux":
 		switch distro.Get() {
 		case distro.NixOS:
@@ -178,20 +180,20 @@ func (up *Updater) getUpdateFunction() (fn updateFunction, canAutoUpdate bool) {
 			// auto-update mechanism.
 			return up.updateSynology, false
 		case distro.Debian: // includes Ubuntu
-			return up.updateDebLike, true
+			return up.updateDebLike, canAutoUpdate
 		case distro.Arch:
 			if up.archPackageInstalled() {
 				// Arch update func just prints a message about how to update,
 				// it doesn't support auto-updates.
 				return up.updateArchLike, false
 			}
-			return up.updateLinuxBinary, true
+			return up.updateLinuxBinary, canAutoUpdate
 		case distro.Alpine:
-			return up.updateAlpineLike, true
+			return up.updateAlpineLike, canAutoUpdate
 		case distro.Unraid:
-			return up.updateUnraid, true
+			return up.updateUnraid, canAutoUpdate
 		case distro.QNAP:
-			return up.updateQNAP, true
+			return up.updateQNAP, canAutoUpdate
 		}
 		switch {
 		case haveExecutable("pacman"):
@@ -200,21 +202,21 @@ func (up *Updater) getUpdateFunction() (fn updateFunction, canAutoUpdate bool) {
 				// it doesn't support auto-updates.
 				return up.updateArchLike, false
 			}
-			return up.updateLinuxBinary, true
+			return up.updateLinuxBinary, canAutoUpdate
 		case haveExecutable("apt-get"): // TODO(awly): add support for "apt"
 			// The distro.Debian switch case above should catch most apt-based
 			// systems, but add this fallback just in case.
-			return up.updateDebLike, true
+			return up.updateDebLike, canAutoUpdate
 		case haveExecutable("dnf"):
-			return up.updateFedoraLike("dnf"), true
+			return up.updateFedoraLike("dnf"), canAutoUpdate
 		case haveExecutable("yum"):
-			return up.updateFedoraLike("yum"), true
+			return up.updateFedoraLike("yum"), canAutoUpdate
 		case haveExecutable("apk"):
-			return up.updateAlpineLike, true
+			return up.updateAlpineLike, canAutoUpdate
 		}
 		// If nothing matched, fall back to tarball updates.
 		if up.Update == nil {
-			return up.updateLinuxBinary, true
+			return up.updateLinuxBinary, canAutoUpdate
 		}
 	case "darwin":
 		switch {
@@ -230,7 +232,7 @@ func (up *Updater) getUpdateFunction() (fn updateFunction, canAutoUpdate bool) {
 			return nil, false
 		}
 	case "freebsd":
-		return up.updateFreeBSD, true
+		return up.updateFreeBSD, canAutoUpdate
 	}
 	return nil, false
 }
diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index d783fa72f..4c57502aa 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -2974,6 +2974,9 @@ func (b *LocalBackend) checkPrefsLocked(p *ipn.Prefs) error {
 	if err := b.checkFunnelEnabledLocked(p); err != nil {
 		errs = append(errs, err)
 	}
+	if err := b.checkAutoUpdatePrefsLocked(p); err != nil {
+		errs = append(errs, err)
+	}
 	return multierr.New(errs...)
 }
 
@@ -3064,6 +3067,13 @@ func (b *LocalBackend) checkFunnelEnabledLocked(p *ipn.Prefs) error {
 	return nil
 }
 
+func (b *LocalBackend) checkAutoUpdatePrefsLocked(p *ipn.Prefs) error {
+	if p.AutoUpdate.Apply.EqualBool(true) && !clientupdate.CanAutoUpdate() {
+		return errors.New("Auto-updates are not supported on this platform.")
+	}
+	return nil
+}
+
 // SetUseExitNodeEnabled turns on or off the most recently selected exit node.
 //
 // On success, it returns the resulting prefs (or current prefs, in the case of no change).
diff --git a/ipn/ipnlocal/local_test.go b/ipn/ipnlocal/local_test.go
index 65fd981a9..c8c658f9d 100644
--- a/ipn/ipnlocal/local_test.go
+++ b/ipn/ipnlocal/local_test.go
@@ -25,6 +25,7 @@
 	"golang.org/x/net/dns/dnsmessage"
 	"tailscale.com/appc"
 	"tailscale.com/appc/appctest"
+	"tailscale.com/clientupdate"
 	"tailscale.com/control/controlclient"
 	"tailscale.com/drive"
 	"tailscale.com/drive/driveimpl"
@@ -3402,3 +3403,39 @@ func TestMinLatencyDERPregion(t *testing.T) {
 		})
 	}
 }
+
+func TestEnableAutoUpdates(t *testing.T) {
+	lb := newTestLocalBackend(t)
+
+	_, err := lb.EditPrefs(&ipn.MaskedPrefs{
+		AutoUpdateSet: ipn.AutoUpdatePrefsMask{
+			ApplySet: true,
+		},
+		Prefs: ipn.Prefs{
+			AutoUpdate: ipn.AutoUpdatePrefs{
+				Apply: opt.NewBool(true),
+			},
+		},
+	})
+	// Enabling may fail, depending on which environment we are running this
+	// test in.
+	wantErr := !clientupdate.CanAutoUpdate()
+	gotErr := err != nil
+	if gotErr != wantErr {
+		t.Fatalf("enabling auto-updates: got error: %v (%v); want error: %v", gotErr, err, wantErr)
+	}
+
+	// Disabling should always succeed.
+	if _, err := lb.EditPrefs(&ipn.MaskedPrefs{
+		AutoUpdateSet: ipn.AutoUpdatePrefsMask{
+			ApplySet: true,
+		},
+		Prefs: ipn.Prefs{
+			AutoUpdate: ipn.AutoUpdatePrefs{
+				Apply: opt.NewBool(false),
+			},
+		},
+	}); err != nil {
+		t.Fatalf("disabling auto-updates: got error: %v", err)
+	}
+}