diff --git a/build-tools/utils/custom-css-properties.js b/build-tools/utils/custom-css-properties.js
index 73511df043..cb51af6453 100644
--- a/build-tools/utils/custom-css-properties.js
+++ b/build-tools/utils/custom-css-properties.js
@@ -155,6 +155,11 @@ const customCssPropertiesList = [
   'promptInputStylePlaceholderFontSize',
   'promptInputStylePlaceholderFontStyle',
   'promptInputStylePlaceholderFontWeight',
+  // Prompt input menu/dropdown style properties
+  'promptInputMenuStyleBackgroundColor',
+  'promptInputMenuStyleBorderColor',
+  'promptInputMenuStyleBorderRadius',
+  'promptInputMenuStyleBorderWidth',
   // Progress bar style properties
   'progressBarBackgroundColor',
   'progressBarBorderRadius',
diff --git a/pages/prompt-input/menu-style.page.tsx b/pages/prompt-input/menu-style.page.tsx
new file mode 100644
index 0000000000..ed707a5263
--- /dev/null
+++ b/pages/prompt-input/menu-style.page.tsx
@@ -0,0 +1,48 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+import React, { useState } from 'react';
+
+import PromptInput, { PromptInputProps } from '~components/prompt-input';
+
+const menuStyle: PromptInputProps.Style['menu'] = {
+  backgroundColor: 'light-dark(#faf5ff, #2d1b4e)',
+  borderColor: '#a78bfa',
+  borderRadius: '12px',
+  borderWidth: '1.5px',
+};
+
+const options: PromptInputProps.MenuDefinition['options'] = [
+  { value: 'help', label: '/help', description: 'Show help' },
+  { value: 'search', label: '/search', description: 'Search content' },
+  { value: 'clear', label: '/clear', description: 'Clear the input' },
+];
+
+export default function MenuStylePage() {
+  const [value, setValue] = useState('');
+  const [tokens, setTokens] = useState<readonly PromptInputProps.InputToken[]>([]);
+
+  return (
+    <>
+      <h1>PromptInput — menu style override</h1>
+      <p>
+        Type <code>/</code> to open the command menu. The dropdown uses the custom <code>style.menu</code> overrides
+        (purple border, rounded corners, themed background).
+      </p>
+      <PromptInput
+        ariaLabel="Prompt input with styled menu"
+        value={value}
+        tokens={tokens}
+        menus={[{ id: 'commands', trigger: '/', options, filteringType: 'auto' }]}
+        style={{ menu: menuStyle }}
+        onChange={({ detail }) => {
+          setValue(detail.value);
+          if (detail.tokens) {
+            setTokens(detail.tokens);
+          }
+        }}
+        onAction={() => {}}
+        i18nStrings={{ actionButtonAriaLabel: 'Send' }}
+      />
+    </>
+  );
+}
diff --git a/src/prompt-input/__tests__/styles.test.tsx b/src/prompt-input/__tests__/styles.test.tsx
index beee993c47..547b0ae51a 100644
--- a/src/prompt-input/__tests__/styles.test.tsx
+++ b/src/prompt-input/__tests__/styles.test.tsx
@@ -60,6 +60,12 @@ describe('getPromptInputStyles', () => {
         fontWeight: '400',
         fontStyle: 'italic',
       },
+      menu: {
+        backgroundColor: '#1a1a2e',
+        borderColor: '#7b2d8b',
+        borderRadius: '12px',
+        borderWidth: '1.5px',
+      },
     };
 
     expect(getPromptInputStyles(allStyles)).toEqual({
@@ -93,6 +99,10 @@ describe('getPromptInputStyles', () => {
       [customCssProps.promptInputStylePlaceholderFontSize]: '14px',
       [customCssProps.promptInputStylePlaceholderFontWeight]: '400',
       [customCssProps.promptInputStylePlaceholderFontStyle]: 'italic',
+      [customCssProps.promptInputMenuStyleBackgroundColor]: '#1a1a2e',
+      [customCssProps.promptInputMenuStyleBorderColor]: '#7b2d8b',
+      [customCssProps.promptInputMenuStyleBorderRadius]: '12px',
+      [customCssProps.promptInputMenuStyleBorderWidth]: '1.5px',
     });
   });
 
diff --git a/src/prompt-input/components/token-mode.tsx b/src/prompt-input/components/token-mode.tsx
index b5716048bc..c6aa8b3e45 100644
--- a/src/prompt-input/components/token-mode.tsx
+++ b/src/prompt-input/components/token-mode.tsx
@@ -4,6 +4,7 @@
 import React from 'react';
 import clsx from 'clsx';
 
+import { DropdownProps } from '../../dropdown/interfaces';
 import Dropdown from '../../dropdown/internal';
 import DropdownFooter from '../../internal/components/dropdown-footer';
 import { DropdownStatusResult } from '../../internal/components/dropdown-status';
@@ -53,6 +54,7 @@ interface TokenModeProps {
   i18nStrings?: PromptInputProps['i18nStrings'];
 
   maxMenuHeight?: number;
+  menuStyle?: PromptInputProps.Style['menu'];
 }
 
 const MENU_MIN_WIDTH = 300;
@@ -76,6 +78,7 @@ export default function TokenMode({
   menuItemsHandlers,
   menuDropdownStatus,
   maxMenuHeight,
+  menuStyle,
   handleInput,
   handleLoadMore,
   editableElementAttributes,
@@ -117,6 +120,19 @@ export default function TokenMode({
           minWidth={MENU_MIN_WIDTH}
           maxHeight={maxMenuHeight}
           expandToViewport={true}
+          style={
+            menuStyle
+              ? ({
+                  // DropdownProps.Style names the fill `background`; PromptInput exposes it as `backgroundColor`.
+                  dropdown: {
+                    background: menuStyle.backgroundColor,
+                    borderColor: menuStyle.borderColor,
+                    borderRadius: menuStyle.borderRadius,
+                    borderWidth: menuStyle.borderWidth,
+                  },
+                } satisfies DropdownProps.Style)
+              : undefined
+          }
           open={
             !!(
               shouldRenderMenuDropdown &&
diff --git a/src/prompt-input/interfaces.ts b/src/prompt-input/interfaces.ts
index 36011abcee..ee7569a7e3 100644
--- a/src/prompt-input/interfaces.ts
+++ b/src/prompt-input/interfaces.ts
@@ -574,5 +574,18 @@ export namespace PromptInputProps {
       fontStyle?: string;
       fontWeight?: string;
     };
+    /**
+     * Style overrides for the menus/shortcuts dropdown that appears when a trigger
+     * character is typed. Use this to match the dropdown's visual appearance to a
+     * custom design system theme.
+     *
+     * @awsuiSystem core
+     */
+    menu?: {
+      backgroundColor?: string;
+      borderColor?: string;
+      borderRadius?: string;
+      borderWidth?: string;
+    };
   }
 }
diff --git a/src/prompt-input/internal.tsx b/src/prompt-input/internal.tsx
index 4a042cc067..716e5e3c80 100644
--- a/src/prompt-input/internal.tsx
+++ b/src/prompt-input/internal.tsx
@@ -444,6 +444,7 @@ const InternalPromptInput = React.forwardRef(
               menuItemsHandlers={tokenMode.menuItemsHandlers}
               menuDropdownStatus={tokenMode.menuDropdownStatus}
               maxMenuHeight={maxMenuHeight}
+              menuStyle={style?.menu}
               handleInput={tokenMode.handleInput}
               handleLoadMore={tokenMode.handleLoadMore}
               editableElementAttributes={tokenMode.editableElementAttributes}
diff --git a/src/prompt-input/styles.tsx b/src/prompt-input/styles.tsx
index f993af759d..ec7013277f 100644
--- a/src/prompt-input/styles.tsx
+++ b/src/prompt-input/styles.tsx
@@ -40,5 +40,9 @@ export function getPromptInputStyles(style: PromptInputProps['style']) {
     [customCssProps.promptInputStylePlaceholderFontSize]: style?.placeholder?.fontSize,
     [customCssProps.promptInputStylePlaceholderFontWeight]: style?.placeholder?.fontWeight,
     [customCssProps.promptInputStylePlaceholderFontStyle]: style?.placeholder?.fontStyle,
+    [customCssProps.promptInputMenuStyleBackgroundColor]: style?.menu?.backgroundColor,
+    [customCssProps.promptInputMenuStyleBorderColor]: style?.menu?.borderColor,
+    [customCssProps.promptInputMenuStyleBorderRadius]: style?.menu?.borderRadius,
+    [customCssProps.promptInputMenuStyleBorderWidth]: style?.menu?.borderWidth,
   };
 }