diff --git a/packages/flutter/lib/src/material/input_decorator.dart b/packages/flutter/lib/src/material/input_decorator.dart
index c54ba8a05a..d957c7aaf2 100644
--- a/packages/flutter/lib/src/material/input_decorator.dart
+++ b/packages/flutter/lib/src/material/input_decorator.dart
@@ -1410,7 +1410,7 @@ class _RenderDecoration extends RenderBox with SlottedContainerRenderObjectMixin
         double start = right - _boxSize(icon).width;
         double end = left;
         if (prefixIcon != null) {
-          start += contentPadding.left;
+          start += contentPadding.right;
           start -= centerLayout(prefixIcon!, start - prefixIcon!.size.width);
         }
         if (label != null) {
diff --git a/packages/flutter/test/material/input_decorator_test.dart b/packages/flutter/test/material/input_decorator_test.dart
index 4d543a8d98..7755053967 100644
--- a/packages/flutter/test/material/input_decorator_test.dart
+++ b/packages/flutter/test/material/input_decorator_test.dart
@@ -6516,5 +6516,35 @@ void main() {
     final Text hintTextWidget = tester.widget(hintTextFinder);
     expect(hintTextWidget.style!.overflow, decoration.hintStyle!.overflow);
   });
+
+  testWidgets('prefixIcon in RTL with asymmetric padding', (WidgetTester tester) async {
+    // Regression test for https://github.com/flutter/flutter/issues/129591
+    const InputDecoration decoration = InputDecoration(
+      contentPadding: EdgeInsetsDirectional.only(end: 24),
+      prefixIcon: Focus(child: Icon(Icons.search)),
+    );
+
+    await tester.pumpWidget(
+      buildInputDecorator(
+        useMaterial3: useMaterial3,
+        // isEmpty: false (default)
+        // isFocused: false (default)
+        decoration: decoration,
+        textDirection: TextDirection.rtl,
+      ),
+    );
+    await tester.pumpAndSettle();
+
+    expect(find.byType(InputDecorator), findsOneWidget);
+    expect(find.byType(Icon), findsOneWidget);
+
+    final Offset(dx: double decoratorRight) =
+        tester.getTopRight(find.byType(InputDecorator));
+    final Offset(dx: double prefixRight) =
+        tester.getTopRight(find.byType(Icon));
+
+    // The prefix is inside the decorator.
+    expect(decoratorRight, lessThanOrEqualTo(prefixRight));
+  });
 }
 }