diff --git a/control/controlclient/direct.go b/control/controlclient/direct.go
index dc3ebd300..fe01a202c 100644
--- a/control/controlclient/direct.go
+++ b/control/controlclient/direct.go
@@ -79,6 +79,7 @@ type Direct struct {
 	autoUpdatePub     *eventbus.Publisher[AutoUpdate]
 	controlTimePub    *eventbus.Publisher[ControlTime]
 	getMachinePrivKey func() (key.MachinePrivate, error)
+	persistState      func(persist.PersistView) // or nil; called before RegisterRequest to persist new node key
 	debugFlags        []string
 	pinger            Pinger
 	popBrowser        func(url string)    // or nil
@@ -176,6 +177,12 @@ type Options struct {
 	// attempted. It is used to allow the client to clean up any resources or complete any
 	// tasks that are dependent on a live client.
 	Shutdown func()
+
+	// PersistState, if non-nil, is called with an updated Persist after
+	// generating a new node key but before sending the RegisterRequest.
+	// This allows the caller to write the key to durable storage so that
+	// a crash during registration doesn't lose the key.
+	PersistState func(persist.PersistView)
 }
 
 // ControlDialPlanner is the interface optionally supplied when creating a
@@ -322,6 +329,7 @@ func NewDirect(opts Options) (*Direct, error) {
 		dialer:            opts.Dialer,
 		dnsCache:          dnsCache,
 		dialPlan:          opts.DialPlan,
+		persistState:      opts.PersistState,
 	}
 	c.discoPubKey = opts.DiscoPublicKey
 	c.closedCtx, c.closeCtx = context.WithCancel(context.Background())
@@ -646,6 +654,14 @@ func (c *Direct) doLogin(ctx context.Context, opt loginOpt) (mustRegen bool, new
 		persist.NetworkLockKey = key.NewNLPrivate()
 	}
 
+	// Persist the new key before the RegisterRequest so a crash
+	// mid-HTTP doesn't lose it.
+	if c.persistState != nil && !tryingNewKey.IsZero() && (persist.PrivateNodeKey.IsZero() || tryingNewKey.Public() != persist.PrivateNodeKey.Public()) {
+		preHTTPPersist := persist
+		preHTTPPersist.PrivateNodeKey = tryingNewKey
+		c.persistState(preHTTPPersist.View())
+	}
+
 	nlPub := persist.NetworkLockKey.Public()
 
 	if tryingNewKey.IsZero() {
diff --git a/ipn/ipnlocal/local.go b/ipn/ipnlocal/local.go
index 845317c4a..267eba301 100644
--- a/ipn/ipnlocal/local.go
+++ b/ipn/ipnlocal/local.go
@@ -2629,6 +2629,7 @@ func (b *LocalBackend) startLocked(opts ipn.Options) error {
 	// but it won't take effect until the next Start.
 	cc, err := b.getNewControlClientFuncLocked()(controlclient.Options{
 		GetMachinePrivateKey: b.createGetMachinePrivateKeyFunc(),
+		PersistState:         b.createPersistStateFunc(),
 		Logf:                 logger.WithPrefix(b.logf, "control: "),
 		Persist:              *persistv,
 		ServerURL:            serverURL,
@@ -3630,6 +3631,21 @@ func (b *LocalBackend) createGetMachinePrivateKeyFunc() func() (key.MachinePriva
 	}
 }
 
+// createPersistStateFunc returns a function that writes an updated Persist
+// directly to the state store, bypassing setPrefsNoPermCheck to avoid
+// triggering hooks for state not yet confirmed by the control server.
+func (b *LocalBackend) createPersistStateFunc() func(persist.PersistView) {
+	return func(p persist.PersistView) {
+		b.mu.Lock()
+		defer b.mu.Unlock()
+		prefs := b.pm.CurrentPrefs().AsStruct()
+		prefs.Persist = p.AsStruct()
+		if err := b.pm.writePrefsToStore(b.pm.currentProfile.Key(), prefs.View()); err != nil {
+			b.logf("persist node key before register: %v", err)
+		}
+	}
+}
+
 // initMachineKeyLocked is called to initialize b.machinePrivKey.
 //
 // b.prefs must already be initialized.