diff --git a/hscontrol/state/persist_test.go b/hscontrol/state/persist_test.go
index e29de839..95064ea4 100644
--- a/hscontrol/state/persist_test.go
+++ b/hscontrol/state/persist_test.go
@@ -1,6 +1,7 @@
 package state
 
 import (
+	"errors"
 	"net/netip"
 	"testing"
 	"time"
@@ -10,6 +11,7 @@ import (
 	"github.com/juanfont/headscale/hscontrol/util"
 	"github.com/stretchr/testify/assert"
 	"github.com/stretchr/testify/require"
+	"gorm.io/gorm"
 	"tailscale.com/tailcfg"
 	"tailscale.com/types/key"
 )
@@ -472,3 +474,55 @@ func TestPreAuthKeyReauthRejectsNodeKeyClaimedByAnotherMachine(t *testing.T) {
 	require.Equal(t, victimMachine.Public(), owner.MachineKey(),
 		"victim's NodeKey index entry must be untouched")
 }
+
+var errInjectedNodeUpdate = errors.New("injected node update failure")
+
+// TestPreAuthKeyReauthRevertsNodeStoreOnDBFailure ensures a failed database
+// write during pre-auth-key re-registration does not leave the NodeStore
+// holding a node key that was never persisted: a restart would reload the old
+// row and the client's current key would no longer resolve, locking it out.
+func TestPreAuthKeyReauthRevertsNodeStoreOnDBFailure(t *testing.T) {
+	dbPath := t.TempDir() + "/headscale.db"
+	cfg := persistTestConfig(dbPath)
+
+	s, err := NewState(cfg)
+	require.NoError(t, err)
+	t.Cleanup(func() { _ = s.Close() })
+
+	user := s.CreateUserForTest("reauth-user")
+
+	pak, err := s.CreatePreAuthKey(user.TypedID(), true, false, nil, nil)
+	require.NoError(t, err)
+
+	machineKey := key.NewMachine()
+	regReq := tailcfg.RegisterRequest{
+		Auth:     &tailcfg.RegisterResponseAuth{AuthKey: pak.Key},
+		NodeKey:  key.NewNode().Public(),
+		Hostinfo: &tailcfg.Hostinfo{Hostname: "reauth-node"},
+		Expiry:   time.Now().Add(24 * time.Hour),
+	}
+	node, _, err := s.HandleNodeFromPreAuthKey(regReq, machineKey.Public())
+	require.NoError(t, err)
+
+	origNodeKey := node.NodeKey()
+
+	// Fail the node row update so the re-registration's database write errors
+	// after the NodeStore has already been mutated.
+	require.NoError(t, s.db.DB.Callback().Update().Before("gorm:update").
+		Register("fail_node_update", func(tx *gorm.DB) {
+			if tx.Statement.Table == "nodes" {
+				_ = tx.AddError(errInjectedNodeUpdate)
+			}
+		}))
+
+	reReg := regReq
+	reReg.NodeKey = key.NewNode().Public() // rotate -> NodeStore mutation, then DB write fails
+	_, _, err = s.HandleNodeFromPreAuthKey(reReg, machineKey.Public())
+	require.NoError(t, s.db.DB.Callback().Update().Remove("fail_node_update"))
+	require.Error(t, err, "re-registration must fail when the database write fails")
+
+	got, ok := s.nodeStore.GetNode(node.ID())
+	require.True(t, ok)
+	require.Equal(t, origNodeKey, got.NodeKey(),
+		"NodeStore must revert to the persisted node key when the write fails")
+}
diff --git a/hscontrol/state/state.go b/hscontrol/state/state.go
index f2803fde..07f1c24e 100644
--- a/hscontrol/state/state.go
+++ b/hscontrol/state/state.go
@@ -2321,6 +2321,12 @@ func (s *State) HandleNodeFromPreAuthKey(
 			return types.NodeView{}, change.Change{}, ErrNodeKeyInUse
 		}
 
+		// Snapshot the pre-update node so the NodeStore can be rolled back if
+		// the database write below fails. The view points at the immutable
+		// pre-update snapshot (UpdateNode swaps in a new one), so this stays
+		// valid after the mutation.
+		priorNode := existingNodeSameUser.AsStruct()
+
 		// Update existing node - NodeStore first, then database
 		updatedNodeView, ok := s.nodeStore.UpdateNode(existingNodeSameUser.ID(), func(node *types.Node) {
 			node.NodeKey = regReq.NodeKey
@@ -2401,6 +2407,13 @@ func (s *State) HandleNodeFromPreAuthKey(
 			return nil, nil //nolint:nilnil // intentional: transaction success
 		})
 		if err != nil {
+			// The NodeStore was updated before the database write. Roll it back
+			// so it does not advertise a registration the database rejected
+			// (e.g. a node key that a restart would not reload).
+			if priorNode != nil {
+				s.nodeStore.PutNode(*priorNode)
+			}
+
 			return types.NodeView{}, change.Change{}, fmt.Errorf("writing node to database: %w", err)
 		}