diff --git a/packages/flutter/lib/src/material/text_field.dart b/packages/flutter/lib/src/material/text_field.dart
index 4a3a1e54186c..9b71adbdc9c6 100644
--- a/packages/flutter/lib/src/material/text_field.dart
+++ b/packages/flutter/lib/src/material/text_field.dart
@@ -1290,6 +1290,7 @@ class _TextFieldState extends State<TextField> with RestorationMixin implements
     Color? autocorrectionTextRectColor;
     Radius? cursorRadius = widget.cursorRadius;
     VoidCallback? handleDidGainAccessibilityFocus;
+    VoidCallback? handleDidLoseAccessibilityFocus;
 
     switch (theme.platform) {
       case TargetPlatform.iOS:
@@ -1320,6 +1321,9 @@ class _TextFieldState extends State<TextField> with RestorationMixin implements
             _effectiveFocusNode.requestFocus();
           }
         };
+        handleDidLoseAccessibilityFocus = () {
+          _effectiveFocusNode.unfocus();
+        };
 
       case TargetPlatform.android:
       case TargetPlatform.fuchsia:
@@ -1337,6 +1341,15 @@ class _TextFieldState extends State<TextField> with RestorationMixin implements
         cursorOpacityAnimates ??= false;
         cursorColor = _hasError ? _errorColor : widget.cursorColor ?? selectionStyle.cursorColor ?? theme.colorScheme.primary;
         selectionColor = selectionStyle.selectionColor ?? theme.colorScheme.primary.withOpacity(0.40);
+        handleDidGainAccessibilityFocus = () {
+          // Automatically activate the TextField when it receives accessibility focus.
+          if (!_effectiveFocusNode.hasFocus && _effectiveFocusNode.canRequestFocus) {
+            _effectiveFocusNode.requestFocus();
+          }
+        };
+        handleDidLoseAccessibilityFocus = () {
+          _effectiveFocusNode.unfocus();
+        };
 
       case TargetPlatform.windows:
         forcePressEnabled = false;
@@ -1351,6 +1364,9 @@ class _TextFieldState extends State<TextField> with RestorationMixin implements
             _effectiveFocusNode.requestFocus();
           }
         };
+        handleDidLoseAccessibilityFocus = () {
+          _effectiveFocusNode.unfocus();
+        };
     }
 
     Widget child = RepaintBoundary(
@@ -1478,6 +1494,7 @@ class _TextFieldState extends State<TextField> with RestorationMixin implements
                   _requestKeyboard();
                 },
                 onDidGainAccessibilityFocus: handleDidGainAccessibilityFocus,
+                onDidLoseAccessibilityFocus: handleDidLoseAccessibilityFocus,
                 child: child,
               );
             },
diff --git a/packages/flutter/test/material/search_test.dart b/packages/flutter/test/material/search_test.dart
index be9a1d6a2498..e1623b664fe8 100644
--- a/packages/flutter/test/material/search_test.dart
+++ b/packages/flutter/test/material/search_test.dart
@@ -605,6 +605,9 @@ void main() {
     const Widget flexibleSpace = Text('FlexibleSpace');
 
     TestSemantics buildExpected({ required String routeName }) {
+      final bool isDesktop = debugDefaultTargetPlatformOverride == TargetPlatform.macOS ||
+          debugDefaultTargetPlatformOverride == TargetPlatform.windows ||
+          debugDefaultTargetPlatformOverride == TargetPlatform.linux;
       return TestSemantics.root(
         children: <TestSemantics>[
           TestSemantics(
@@ -651,9 +654,10 @@ void main() {
                                     debugDefaultTargetPlatformOverride != TargetPlatform.macOS) SemanticsFlag.namesRoute,
                                 ],
                                 actions: <SemanticsAction>[
-                                  if (debugDefaultTargetPlatformOverride == TargetPlatform.macOS ||
-                                    debugDefaultTargetPlatformOverride == TargetPlatform.windows)
+                                  if (isDesktop)
                                     SemanticsAction.didGainAccessibilityFocus,
+                                  if (isDesktop)
+                                    SemanticsAction.didLoseAccessibilityFocus,
                                   SemanticsAction.tap,
                                   SemanticsAction.setSelection,
                                   SemanticsAction.setText,
@@ -748,6 +752,9 @@ void main() {
 
   group('contributes semantics', () {
     TestSemantics buildExpected({ required String routeName }) {
+      final bool isDesktop = debugDefaultTargetPlatformOverride == TargetPlatform.macOS ||
+                             debugDefaultTargetPlatformOverride == TargetPlatform.windows ||
+                             debugDefaultTargetPlatformOverride == TargetPlatform.linux;
       return TestSemantics.root(
         children: <TestSemantics>[
           TestSemantics(
@@ -791,9 +798,10 @@ void main() {
                                 debugDefaultTargetPlatformOverride != TargetPlatform.macOS) SemanticsFlag.namesRoute,
                             ],
                             actions: <SemanticsAction>[
-                              if (debugDefaultTargetPlatformOverride == TargetPlatform.macOS ||
-                                debugDefaultTargetPlatformOverride == TargetPlatform.windows)
+                              if (isDesktop)
                                 SemanticsAction.didGainAccessibilityFocus,
+                              if (isDesktop)
+                                SemanticsAction.didLoseAccessibilityFocus,
                               SemanticsAction.tap,
                               SemanticsAction.setSelection,
                               SemanticsAction.setText,
diff --git a/packages/flutter/test/material/text_field_test.dart b/packages/flutter/test/material/text_field_test.dart
index b7a226e989f1..09fb36bce0f0 100644
--- a/packages/flutter/test/material/text_field_test.dart
+++ b/packages/flutter/test/material/text_field_test.dart
@@ -655,7 +655,7 @@ void main() {
     expect(editableText.cursorOpacityAnimates, false);
   });
 
-  testWidgets('Activates the text field when receives semantics focus on Mac, Windows', (WidgetTester tester) async {
+  testWidgets('Activates the text field when receives semantics focus on desktops', (WidgetTester tester) async {
     final SemanticsTester semantics = SemanticsTester(tester);
     final SemanticsOwner semanticsOwner = tester.binding.pipelineOwner.semanticsOwner!;
     final FocusNode focusNode = FocusNode();
@@ -686,6 +686,7 @@ void main() {
                         actions: <SemanticsAction>[
                           SemanticsAction.tap,
                           SemanticsAction.didGainAccessibilityFocus,
+                          SemanticsAction.didLoseAccessibilityFocus,
                         ],
                         textDirection: TextDirection.ltr,
                       ),
@@ -705,8 +706,12 @@ void main() {
     semanticsOwner.performAction(4, SemanticsAction.didGainAccessibilityFocus);
     await tester.pumpAndSettle();
     expect(focusNode.hasFocus, isTrue);
+
+    semanticsOwner.performAction(4, SemanticsAction.didLoseAccessibilityFocus);
+    await tester.pumpAndSettle();
+    expect(focusNode.hasFocus, isFalse);
     semantics.dispose();
-  }, variant: const TargetPlatformVariant(<TargetPlatform>{ TargetPlatform.macOS, TargetPlatform.windows }));
+  }, variant: const TargetPlatformVariant(<TargetPlatform>{ TargetPlatform.macOS, TargetPlatform.windows, TargetPlatform.linux }));
 
   testWidgets('TextField passes onEditingComplete to EditableText', (WidgetTester tester) async {
     void onEditingComplete() { }