diff --git a/packages/flutter/lib/src/cupertino/theme.dart b/packages/flutter/lib/src/cupertino/theme.dart
index b4daa961c1..b7c7631e2a 100644
--- a/packages/flutter/lib/src/cupertino/theme.dart
+++ b/packages/flutter/lib/src/cupertino/theme.dart
@@ -130,7 +130,7 @@ class CupertinoTheme extends StatelessWidget {
   }
 }
 
-class _InheritedCupertinoTheme extends InheritedWidget {
+class _InheritedCupertinoTheme extends InheritedTheme {
   const _InheritedCupertinoTheme({
     required this.theme,
     required super.child,
@@ -138,6 +138,11 @@ class _InheritedCupertinoTheme extends InheritedWidget {
 
   final CupertinoTheme theme;
 
+  @override
+  Widget wrap(BuildContext context, Widget child) {
+    return CupertinoTheme(data: theme.data, child: child);
+  }
+
   @override
   bool updateShouldNotify(_InheritedCupertinoTheme old) => theme.data != old.theme.data;
 }
diff --git a/packages/flutter/lib/src/widgets/text_selection.dart b/packages/flutter/lib/src/widgets/text_selection.dart
index e83f266ce4..a7b6b75943 100644
--- a/packages/flutter/lib/src/widgets/text_selection.dart
+++ b/packages/flutter/lib/src/widgets/text_selection.dart
@@ -21,6 +21,7 @@ import 'debug.dart';
 import 'editable_text.dart';
 import 'framework.dart';
 import 'gesture_detector.dart';
+import 'inherited_theme.dart';
 import 'magnifier.dart';
 import 'overlay.dart';
 import 'scrollable.dart';
@@ -1375,12 +1376,22 @@ class SelectionOverlay {
       return;
     }
 
-    _handles = (
-      start: OverlayEntry(builder: _buildStartHandle),
-      end: OverlayEntry(builder: _buildEndHandle),
+    final OverlayState overlay = Overlay.of(context, rootOverlay: true, debugRequiredFor: debugRequiredFor);
+
+    final CapturedThemes capturedThemes = InheritedTheme.capture(
+      from: context,
+      to: overlay.context,
     );
-    Overlay.of(context, rootOverlay: true, debugRequiredFor: debugRequiredFor)
-        .insertAll(<OverlayEntry>[_handles!.start, _handles!.end]);
+
+    _handles = (
+      start: OverlayEntry(builder: (BuildContext context) {
+        return capturedThemes.wrap(_buildStartHandle(context));
+      }),
+      end: OverlayEntry(builder: (BuildContext context) {
+        return capturedThemes.wrap(_buildEndHandle(context));
+      }),
+    );
+    overlay.insertAll(<OverlayEntry>[_handles!.start, _handles!.end]);
   }
 
   /// {@template flutter.widgets.SelectionOverlay.hideHandles}
diff --git a/packages/flutter/test/cupertino/text_field_test.dart b/packages/flutter/test/cupertino/text_field_test.dart
index 98d73d235f..002c8a2afb 100644
--- a/packages/flutter/test/cupertino/text_field_test.dart
+++ b/packages/flutter/test/cupertino/text_field_test.dart
@@ -621,6 +621,47 @@ void main() {
     },
   );
 
+  testWidgets('selection handles color respects CupertinoTheme', (WidgetTester tester) async {
+    // Regression test for https://github.com/flutter/flutter/issues/74890.
+    const Color expectedSelectionHandleColor = Color.fromARGB(255, 10, 200, 255);
+
+    final TextEditingController controller = TextEditingController(text: 'Some text.');
+
+    await tester.pumpWidget(
+      CupertinoApp(
+        theme: const CupertinoThemeData(
+          primaryColor: Colors.red,
+        ),
+        home: Center(
+          child: CupertinoTheme(
+            data: const CupertinoThemeData(
+              primaryColor: expectedSelectionHandleColor,
+            ),
+            child: CupertinoTextField(controller: controller),
+          ),
+        ),
+      ),
+    );
+
+    await tester.tapAt(textOffsetToPosition(tester, 0));
+    await tester.pump();
+    await tester.tapAt(textOffsetToPosition(tester, 0));
+    await tester.pumpAndSettle();
+    final Iterable<RenderBox> boxes = tester.renderObjectList<RenderBox>(
+      find.descendant(
+        of: find.byWidgetPredicate((Widget w) => '${w.runtimeType}' == '_SelectionHandleOverlay'),
+        matching: find.byType(CustomPaint),
+      ),
+    );
+    expect(boxes.length, 2);
+
+    for (final RenderBox box in boxes) {
+      expect(box, paints..path(color: expectedSelectionHandleColor));
+    }
+  },
+    variant: TargetPlatformVariant.only(TargetPlatform.iOS),
+  );
+
   testWidgets(
     'uses DefaultSelectionStyle for selection and cursor colors if provided',
     (WidgetTester tester) async {
diff --git a/packages/flutter/test/material/text_field_test.dart b/packages/flutter/test/material/text_field_test.dart
index 477da112ec..cea5f25ac0 100644
--- a/packages/flutter/test/material/text_field_test.dart
+++ b/packages/flutter/test/material/text_field_test.dart
@@ -9292,6 +9292,49 @@ void main() {
     expect(editableText.style.color, isNull);
   });
 
+  testWidgets('selection handles color respects Theme', (WidgetTester tester) async {
+    // Regression test for https://github.com/flutter/flutter/issues/74890.
+    const Color expectedSelectionHandleColor = Color.fromARGB(255, 10, 200, 255);
+
+    final TextEditingController controller = TextEditingController(text: 'Some text.');
+
+    await tester.pumpWidget(
+      MaterialApp(
+        theme: ThemeData(
+          textSelectionTheme: const TextSelectionThemeData(
+            selectionHandleColor: Colors.red,
+          ),
+        ),
+        home: Material(
+          child: Theme(
+            data: ThemeData(
+              textSelectionTheme: const TextSelectionThemeData(
+                selectionHandleColor: expectedSelectionHandleColor,
+              ),
+            ),
+            child: TextField(controller: controller),
+          ),
+        ),
+      ),
+    );
+
+    await tester.longPressAt(textOffsetToPosition(tester, 0));
+    await tester.pumpAndSettle();
+    final Iterable<RenderBox> boxes = tester.renderObjectList<RenderBox>(
+      find.descendant(
+        of: find.byWidgetPredicate((Widget w) => '${w.runtimeType}' == '_SelectionHandleOverlay'),
+        matching: find.byType(CustomPaint),
+      ),
+    );
+    expect(boxes.length, 2);
+
+    for (final RenderBox box in boxes) {
+      expect(box, paints..path(color: expectedSelectionHandleColor));
+    }
+  },
+    variant: const TargetPlatformVariant(<TargetPlatform>{ TargetPlatform.android, TargetPlatform.fuchsia }),
+  );
+
   testWidgets('style enforces required fields', (WidgetTester tester) async {
     Widget buildFrame(TextStyle style) {
       return MaterialApp(