diff --git a/packages/flutter/lib/src/widgets/focus_manager.dart b/packages/flutter/lib/src/widgets/focus_manager.dart
index 24cae56d862..bf4cc7552d4 100644
--- a/packages/flutter/lib/src/widgets/focus_manager.dart
+++ b/packages/flutter/lib/src/widgets/focus_manager.dart
@@ -432,7 +432,7 @@ class FocusNode with DiagnosticableTreeMixin, ChangeNotifier {
   /// arguments must not be null.
   FocusNode({
     String? debugLabel,
-    FocusOnKeyCallback? onKey,
+    this.onKey,
     bool skipTraversal = false,
     bool canRequestFocus = true,
     bool descendantsAreFocusable = true,
@@ -441,8 +441,7 @@ class FocusNode with DiagnosticableTreeMixin, ChangeNotifier {
         assert(descendantsAreFocusable != null),
         _skipTraversal = skipTraversal,
         _canRequestFocus = canRequestFocus,
-        _descendantsAreFocusable = descendantsAreFocusable,
-        _onKey = onKey {
+        _descendantsAreFocusable = descendantsAreFocusable {
     // Set it via the setter so that it does nothing on release builds.
     this.debugLabel = debugLabel;
   }
@@ -573,8 +572,7 @@ class FocusNode with DiagnosticableTreeMixin, ChangeNotifier {
   /// [hasFocus] returns true).
   ///
   /// {@macro flutter.widgets.FocusNode.keyEvents}
-  FocusOnKeyCallback? get onKey => _onKey;
-  FocusOnKeyCallback? _onKey;
+  FocusOnKeyCallback? onKey;
 
   FocusManager? _manager;
   List<FocusNode>? _ancestors;
@@ -1028,7 +1026,7 @@ class FocusNode with DiagnosticableTreeMixin, ChangeNotifier {
   @mustCallSuper
   FocusAttachment attach(BuildContext? context, {FocusOnKeyCallback? onKey}) {
     _context = context;
-    _onKey = onKey ?? _onKey;
+    this.onKey = onKey ?? this.onKey;
     _attachment = FocusAttachment._(this);
     return _attachment!;
   }
diff --git a/packages/flutter/lib/src/widgets/focus_scope.dart b/packages/flutter/lib/src/widgets/focus_scope.dart
index ce4520673a8..fdc50c25aaa 100644
--- a/packages/flutter/lib/src/widgets/focus_scope.dart
+++ b/packages/flutter/lib/src/widgets/focus_scope.dart
@@ -643,6 +643,9 @@ class _FocusState extends State<Focus> {
     }());
 
     if (oldWidget.focusNode == widget.focusNode) {
+      if (widget.onKey != focusNode.onKey) {
+        focusNode.onKey = widget.onKey;
+      }
       if (widget.skipTraversal != null) {
         focusNode.skipTraversal = widget.skipTraversal!;
       }
diff --git a/packages/flutter/test/widgets/focus_scope_test.dart b/packages/flutter/test/widgets/focus_scope_test.dart
index a02c692d8dd..4b378af2bc2 100644
--- a/packages/flutter/test/widgets/focus_scope_test.dart
+++ b/packages/flutter/test/widgets/focus_scope_test.dart
@@ -4,9 +4,10 @@
 
 import 'dart:ui';
 
-import 'package:flutter_test/flutter_test.dart';
-import 'package:flutter/widgets.dart';
 import 'package:flutter/semantics.dart';
+import 'package:flutter/services.dart';
+import 'package:flutter/widgets.dart';
+import 'package:flutter_test/flutter_test.dart';
 
 import 'semantics_tester.dart';
 
@@ -1593,6 +1594,37 @@ void main() {
       final TestSemantics expectedSemantics = TestSemantics.root();
       expect(semantics, hasSemantics(expectedSemantics));
     });
+    testWidgets('Focus updates the onKey handler when the widget updates', (WidgetTester tester) async {
+      final GlobalKey key1 = GlobalKey(debugLabel: '1');
+      final FocusNode focusNode = FocusNode();
+      bool? keyEventHandled;
+      await tester.pumpWidget(
+        Focus(
+          onKey: (_, __) => true, // This one does nothing.
+          focusNode: focusNode,
+          child: Container(key: key1),
+        ),
+      );
+
+      Focus.of(key1.currentContext!).requestFocus();
+      await tester.pump();
+      await tester.sendKeyEvent(LogicalKeyboardKey.enter);
+      expect(keyEventHandled, isNull);
+
+      await tester.pumpWidget(
+        Focus(
+          onKey: (FocusNode node, RawKeyEvent event) { // The updated handler handles the key.
+            keyEventHandled = true;
+            return true;
+          },
+          focusNode: focusNode,
+          child: Container(key: key1),
+        ),
+      );
+
+      await tester.sendKeyEvent(LogicalKeyboardKey.enter);
+      expect(keyEventHandled, isTrue);
+    });
   });
   group('ExcludeFocus', () {
     testWidgets("Descendants of ExcludeFocus aren't focusable.", (WidgetTester tester) async {