diff --git a/packages/flutter/lib/src/material/dropdown_menu_form_field.dart b/packages/flutter/lib/src/material/dropdown_menu_form_field.dart
index d3616b70d98..8eb425f82cb 100644
--- a/packages/flutter/lib/src/material/dropdown_menu_form_field.dart
+++ b/packages/flutter/lib/src/material/dropdown_menu_form_field.dart
@@ -96,7 +96,7 @@ class DropdownMenuFormField<T> extends FormField<T> {
                textAlign: textAlign,
                inputDecorationTheme: inputDecorationTheme,
                menuStyle: menuStyle,
-               controller: controller,
+               controller: state.textFieldController,
                initialSelection: state.value,
                onSelected: field.didChange,
                focusNode: focusNode,
@@ -139,8 +139,14 @@ class DropdownMenuFormField<T> extends FormField<T> {
 class _DropdownMenuFormFieldState<T> extends FormFieldState<T> {
   DropdownMenuFormField<T> get _dropdownMenuFormField => widget as DropdownMenuFormField<T>;
 
+  // The controller used to restore the selected item.
   RestorableTextEditingController? _restorableController;
 
+  // The controller used to reset the content of the DropdownMenu inner TextField.
+  TextEditingController? _localTextFieldController;
+  TextEditingController get textFieldController =>
+      _dropdownMenuFormField.controller ?? (_localTextFieldController ??= TextEditingController());
+
   @override
   void initState() {
     super.initState();
@@ -163,11 +169,16 @@ class _DropdownMenuFormFieldState<T> extends FormFieldState<T> {
     if (oldWidget.initialValue != widget.initialValue && !hasInteractedByUser) {
       setValue(widget.initialValue);
     }
+    if (oldWidget.controller != _dropdownMenuFormField.controller) {
+      _localTextFieldController?.dispose();
+      _localTextFieldController = null;
+    }
   }
 
   @override
   void dispose() {
     _restorableController?.dispose();
+    _localTextFieldController?.dispose();
     super.dispose();
   }
 
@@ -183,6 +194,9 @@ class _DropdownMenuFormFieldState<T> extends FormFieldState<T> {
     super.reset();
     _dropdownMenuFormField.onSelected?.call(value);
     _updateRestorableController(widget.initialValue);
+    if (widget.initialValue == null) {
+      textFieldController.clear();
+    }
   }
 
   void _updateRestorableController(T? value) {
diff --git a/packages/flutter/test/material/dropdown_menu_form_field_test.dart b/packages/flutter/test/material/dropdown_menu_form_field_test.dart
index 14a6ab92216..4f884b504e3 100644
--- a/packages/flutter/test/material/dropdown_menu_form_field_test.dart
+++ b/packages/flutter/test/material/dropdown_menu_form_field_test.dart
@@ -506,13 +506,14 @@ void main() {
       ),
     );
 
-    // Check default value.
-    DropdownMenu<MenuItem> dropdownMenu = tester.widget(find.byType(DropdownMenu<MenuItem>));
-    expect(dropdownMenu.controller, null);
-
     final TextEditingController controller = TextEditingController();
     addTearDown(controller.dispose);
 
+    // Check default value.
+    DropdownMenu<MenuItem> dropdownMenu = tester.widget(find.byType(DropdownMenu<MenuItem>));
+    expect(dropdownMenu.controller, isNotNull); // A default controller is created.
+    expect(dropdownMenu.controller, isNot(controller));
+
     await tester.pumpWidget(
       MaterialApp(
         home: Scaffold(
@@ -967,6 +968,92 @@ void main() {
     expect(fieldKey.currentState!.value, MenuItem.menuItem0);
   });
 
+  // Regression test for https://github.com/flutter/flutter/issues/174578.
+  testWidgets(
+    'Inner text field is cleared on reset when initialSelection is null - Default controller',
+    (WidgetTester tester) async {
+      final GlobalKey<FormFieldState<MenuItem>> fieldKey = GlobalKey<FormFieldState<MenuItem>>();
+
+      await tester.pumpWidget(
+        MaterialApp(
+          home: Scaffold(
+            body: DropdownMenuFormField<MenuItem>(key: fieldKey, dropdownMenuEntries: menuEntries),
+          ),
+        ),
+      );
+
+      final TextField textField = tester.widget(find.byType(TextField));
+
+      // Select menuItem1.
+      await tester.tap(find.byType(DropdownMenu<MenuItem>));
+      await tester.pump();
+      await tester.tap(findMenuItem(MenuItem.menuItem1));
+      await tester.pump();
+      expect(fieldKey.currentState!.value, MenuItem.menuItem1);
+      expect(
+        textField.controller?.value,
+        const TextEditingValue(text: 'Item 1', selection: TextSelection.collapsed(offset: 6)),
+      );
+
+      // After reset the text field content is cleared.
+      fieldKey.currentState!.reset();
+      await tester.pump();
+
+      expect(fieldKey.currentState!.value, null);
+      expect(
+        textField.controller?.value,
+        const TextEditingValue(selection: TextSelection.collapsed(offset: 0)),
+      );
+    },
+  );
+
+  // Regression test for https://github.com/flutter/flutter/issues/174578.
+  testWidgets(
+    'Inner text field is cleared on reset when initialSelection is null - Custom controller',
+    (WidgetTester tester) async {
+      final GlobalKey<FormFieldState<MenuItem>> fieldKey = GlobalKey<FormFieldState<MenuItem>>();
+      final TextEditingController controller = TextEditingController();
+      addTearDown(controller.dispose);
+
+      await tester.pumpWidget(
+        MaterialApp(
+          home: Scaffold(
+            body: DropdownMenuFormField<MenuItem>(
+              key: fieldKey,
+              controller: controller,
+              dropdownMenuEntries: menuEntries,
+            ),
+          ),
+        ),
+      );
+
+      // Custom controller is correctly passed to the inner TextField.
+      final TextField textField = tester.widget(find.byType(TextField));
+      expect(textField.controller, controller);
+
+      // Select menuItem1.
+      await tester.tap(find.byType(DropdownMenu<MenuItem>));
+      await tester.pump();
+      await tester.tap(findMenuItem(MenuItem.menuItem1));
+      await tester.pump();
+      expect(fieldKey.currentState!.value, MenuItem.menuItem1);
+      expect(
+        textField.controller?.value,
+        const TextEditingValue(text: 'Item 1', selection: TextSelection.collapsed(offset: 6)),
+      );
+
+      // After reset the text field content is cleared.
+      fieldKey.currentState!.reset();
+      await tester.pump();
+
+      expect(fieldKey.currentState!.value, null);
+      expect(
+        controller.value,
+        const TextEditingValue(selection: TextSelection.collapsed(offset: 0)),
+      );
+    },
+  );
+
   testWidgets('isValid and hasError results are correct', (WidgetTester tester) async {
     final GlobalKey<FormFieldState<MenuItem>> fieldKey = GlobalKey<FormFieldState<MenuItem>>();