diff --git a/pages/app-layout/disable-paddings-breadcrumbs.page.tsx b/pages/app-layout/disable-paddings-breadcrumbs.page.tsx
index e9d78921b7..aa1a396897 100644
--- a/pages/app-layout/disable-paddings-breadcrumbs.page.tsx
+++ b/pages/app-layout/disable-paddings-breadcrumbs.page.tsx
@@ -1,7 +1,6 @@
 // Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
 // SPDX-License-Identifier: Apache-2.0
 import React from 'react';
-import clsx from 'clsx';
 
 import AppLayout from '~components/app-layout';
 import Box from '~components/box';
@@ -17,7 +16,7 @@ export default function () {
       <AppLayout
         ariaLabels={labels}
         disableContentPaddings={true}
-        breadcrumbs={<div className={clsx(styles.highlightBorder, styles.textContent)}>Breadcrumbs</div>}
+        breadcrumbs={<div className={styles.highlightBorder}>Breadcrumbs</div>}
         notifications={
           <div className={styles.highlightBorder}>
             <Box variant="h2">Notifications</Box>
diff --git a/pages/app-layout/runtime-drawers-persist-open-state.page.tsx b/pages/app-layout/runtime-drawers-persist-open-state.page.tsx
new file mode 100644
index 0000000000..d23fdcb162
--- /dev/null
+++ b/pages/app-layout/runtime-drawers-persist-open-state.page.tsx
@@ -0,0 +1,64 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+import React, { useState } from 'react';
+import { render, unmountComponentAtNode } from 'react-dom';
+
+import AppLayout from '~components/app-layout';
+import Header from '~components/header';
+import HelpPanel from '~components/help-panel';
+import awsuiPlugins from '~components/internal/plugins';
+
+import { Breadcrumbs, Counter } from './utils/content-blocks';
+import appLayoutLabels from './utils/labels';
+
+awsuiPlugins.appLayout.registerDrawer({
+  id: 'runtime-drawer-persist-open-state',
+  type: 'global',
+
+  trigger: {
+    iconSvg: `<svg viewBox="0 0 16 16" focusable="false">
+      <circle stroke-width="2" stroke="currentColor" fill="none" cx="8" cy="8" r="7" />
+      <rect fill="currentColor" x="5" y="5" width="6" height="6" />
+    </svg>`,
+  },
+
+  ariaLabels: {
+    closeButton: 'Close button',
+    content: 'Content',
+    triggerButton: 'Trigger button',
+    resizeHandle: 'Resize handle',
+  },
+
+  mountContent: (container, { onVisibilityChange }) => {
+    awsuiPlugins.appLayout.updateDrawer({ id: 'runtime-drawer-persist-open-state', defaultActive: true });
+    onVisibilityChange(isVisible => {
+      awsuiPlugins.appLayout.updateDrawer({ id: 'runtime-drawer-persist-open-state', defaultActive: isVisible });
+    });
+    render(<Counter id="runtime-drawer-persist-open-state" />, container);
+  },
+  unmountContent: container => {
+    unmountComponentAtNode(container);
+  },
+});
+
+export default function () {
+  const [key, setKey] = useState(0);
+  return (
+    <AppLayout
+      key={key}
+      ariaLabels={appLayoutLabels}
+      breadcrumbs={<Breadcrumbs />}
+      content={
+        <>
+          <Header variant="h1" description="This drawer can automatically reopen after app layout instance changes">
+            Drawer with state persistence
+          </Header>
+          <button data-testid="remount-app-layout" onClick={() => setKey(key => key + 1)}>
+            Remount app layout
+          </button>
+        </>
+      }
+      tools={<HelpPanel header={<h2>Info</h2>}>Here is some info for you</HelpPanel>}
+    />
+  );
+}
diff --git a/pages/app-layout/stateful.page.tsx b/pages/app-layout/stateful.page.tsx
index 3f34f9abc3..c9c3d00aa2 100644
--- a/pages/app-layout/stateful.page.tsx
+++ b/pages/app-layout/stateful.page.tsx
@@ -1,26 +1,13 @@
 // Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
 // SPDX-License-Identifier: Apache-2.0
-import React, { useState } from 'react';
+import React from 'react';
 
 import AppLayout from '~components/app-layout';
 import Header from '~components/header';
 
+import { Counter } from './utils/content-blocks';
 import labels from './utils/labels';
 
-import styles from './styles.scss';
-
-function Counter({ id }: { id: string }) {
-  const [count, setCount] = useState(0);
-  return (
-    <div className={styles.textContent}>
-      <span id={`${id}-text`}>Clicked: {count}</span>
-      <button id={`${id}-button`} onClick={() => setCount(count + 1)}>
-        Click me
-      </button>
-    </div>
-  );
-}
-
 export default function AppLayoutStatefulDemo() {
   return (
     <AppLayout
diff --git a/pages/app-layout/styles.scss b/pages/app-layout/styles.scss
index 597b003c85..020694d140 100644
--- a/pages/app-layout/styles.scss
+++ b/pages/app-layout/styles.scss
@@ -35,10 +35,6 @@
   border-inline: 1px solid red;
 }
 
-.textContent {
-  color: awsui.$color-text-body-default;
-}
-
 .longContent {
   block-size: 200vh;
 }
diff --git a/pages/app-layout/utils/content-blocks.tsx b/pages/app-layout/utils/content-blocks.tsx
index 8145c7538b..b1ca229395 100644
--- a/pages/app-layout/utils/content-blocks.tsx
+++ b/pages/app-layout/utils/content-blocks.tsx
@@ -195,3 +195,15 @@ export function CustomDrawerContent() {
     </div>
   );
 }
+
+export function Counter({ id }: { id: string }) {
+  const [count, setCount] = useState(0);
+  return (
+    <div>
+      <span id={`${id}-text`}>Clicked: {count}</span>
+      <button id={`${id}-button`} onClick={() => setCount(count + 1)}>
+        Click me
+      </button>
+    </div>
+  );
+}
diff --git a/pages/app-layout/utils/external-widget.tsx b/pages/app-layout/utils/external-widget.tsx
index 0cf2090b05..5ea723dfda 100644
--- a/pages/app-layout/utils/external-widget.tsx
+++ b/pages/app-layout/utils/external-widget.tsx
@@ -6,7 +6,7 @@ import ReactDOM, { unmountComponentAtNode } from 'react-dom';
 import Drawer from '~components/drawer';
 import awsuiPlugins from '~components/internal/plugins';
 
-import { CustomDrawerContent } from './content-blocks';
+import { Counter, CustomDrawerContent } from './content-blocks';
 
 const searchParams = new URL(location.hash.substring(1), location.href).searchParams;
 
@@ -84,18 +84,6 @@ awsuiPlugins.appLayout.registerDrawer({
   unmountContent: container => unmountComponentAtNode(container),
 });
 
-const Counter: React.FC = ({ children }) => {
-  const [count, setCount] = useState(0);
-
-  return (
-    <div>
-      <span data-testid="count">{count}</span>
-      <button onClick={() => setCount(count + 1)}>+</button>
-      {children}
-    </div>
-  );
-};
-
 const AutoIncrementCounter: React.FC<{
   onVisibilityChange?: (callback: (isVisible: boolean) => void) => void;
 }> = ({ children, onVisibilityChange }) => {
@@ -192,7 +180,13 @@ awsuiPlugins.appLayout.registerDrawer({
   },
 
   mountContent: container => {
-    ReactDOM.render(<Counter>global widget content circle 2</Counter>, container);
+    ReactDOM.render(
+      <>
+        <Counter id="circle2-global" />
+        global widget content circle 2
+      </>,
+      container
+    );
   },
   unmountContent: container => unmountComponentAtNode(container),
 });
@@ -219,7 +213,13 @@ awsuiPlugins.appLayout.registerDrawer({
   },
 
   mountContent: container => {
-    ReactDOM.render(<Counter>global widget content circle 3</Counter>, container);
+    ReactDOM.render(
+      <>
+        <Counter id="circle3-global" />
+        global widget content circle 3
+      </>,
+      container
+    );
   },
   unmountContent: container => unmountComponentAtNode(container),
 });
diff --git a/src/file-upload/internal.tsx b/src/file-upload/internal.tsx
index c6bd6760fa..460f9d029e 100644
--- a/src/file-upload/internal.tsx
+++ b/src/file-upload/internal.tsx
@@ -9,9 +9,9 @@ import { warnOnce } from '@cloudscape-design/component-toolkit/internal';
 import InternalBox from '../box/internal';
 import { ButtonProps } from '../button/interfaces';
 import { useFormFieldContext } from '../contexts/form-field';
-import InternalFileInput from '../file-input/internal';
 import InternalFileDropzone from '../file-dropzone/internal';
 import { useFilesDragging } from '../file-dropzone/use-files-dragging';
+import InternalFileInput from '../file-input/internal';
 import InternalFileTokenGroup from '../file-token-group/internal';
 import { ConstraintText, FormFieldError, FormFieldWarning } from '../form-field/internal';
 import { getBaseProps } from '../internal/base-component';
diff --git a/src/internal/plugins/controllers/__tests__/drawers.test.ts b/src/internal/plugins/controllers/__tests__/drawers.test.ts
index 2ac9631596..21160fa7a8 100644
--- a/src/internal/plugins/controllers/__tests__/drawers.test.ts
+++ b/src/internal/plugins/controllers/__tests__/drawers.test.ts
@@ -66,12 +66,25 @@ describe('update drawer', () => {
     expect(onDrawersRegistered).not.toHaveBeenCalled();
     await delay();
     expect(onDrawersRegistered).toHaveBeenCalledWith([drawerA, drawerB]);
-    const updatedDrawer = { ...drawerA, badge: true };
+    const updatedDrawer = { ...drawerA, badge: true, defaultActive: true };
     drawers.updateDrawer(updatedDrawer);
     await delay();
     expect(onDrawersRegistered).toHaveBeenLastCalledWith([updatedDrawer, drawerB]);
   });
 
+  test('does not update an unknown property', async () => {
+    const onDrawersRegistered = jest.fn();
+    const drawers = new DrawersController();
+    drawers.onDrawersRegistered(onDrawersRegistered);
+    drawers.registerDrawer(drawerA);
+    await delay();
+    expect(onDrawersRegistered).toHaveBeenCalledWith([drawerA]);
+    const updatedDrawer = { ...drawerA, type: 'global' };
+    drawers.updateDrawer(updatedDrawer);
+    await delay();
+    expect(onDrawersRegistered).toHaveBeenLastCalledWith([drawerA]);
+  });
+
   test('throw error if the update drawer is not registered', () => {
     const drawers = new DrawersController();
     expect(() => drawers.updateDrawer({ id: 'test-drawer' } as UpdateDrawerConfig)).toThrowError(
diff --git a/src/internal/plugins/controllers/drawers.ts b/src/internal/plugins/controllers/drawers.ts
index b63268c802..c7ff534d57 100644
--- a/src/internal/plugins/controllers/drawers.ts
+++ b/src/internal/plugins/controllers/drawers.ts
@@ -32,7 +32,18 @@ export interface DrawerConfig {
   preserveInactiveContent?: boolean;
 }
 
-export type UpdateDrawerConfig = Pick<DrawerConfig, 'id' | 'badge' | 'resizable' | 'defaultSize'>;
+const updatableProperties = [
+  'badge',
+  'resizable',
+  'defaultSize',
+  'orderPriority',
+  'defaultActive',
+  'onResize',
+] as const;
+
+export type UpdateDrawerConfig = { id: DrawerConfig['id'] } & Partial<
+  Pick<DrawerConfig, (typeof updatableProperties)[number]>
+>;
 
 export type DrawersRegistrationListener = (drawers: Array<DrawerConfig>) => void;
 
@@ -67,29 +78,22 @@ export class DrawersController {
     this.scheduleUpdate();
   };
 
-  updateDrawer = (config: UpdateDrawerConfig) => {
-    const { id: drawerId, resizable, badge, defaultSize } = config;
+  updateDrawer = ({ id: drawerId, ...rest }: UpdateDrawerConfig) => {
     const drawerIndex = this.drawers.findIndex(({ id }) => id === drawerId);
     const oldDrawerConfig = this.drawers?.[drawerIndex];
-    if (drawerIndex >= 0 && oldDrawerConfig) {
-      const drawers = this.drawers.slice();
-      const drawerConfig = { ...oldDrawerConfig };
-      if (typeof resizable === 'boolean') {
-        drawerConfig.resizable = resizable;
-      }
-      if (typeof badge === 'boolean') {
-        drawerConfig.badge = badge;
-      }
-      if (typeof defaultSize === 'number') {
-        drawerConfig.defaultSize = defaultSize;
-      }
-
-      drawers[drawerIndex] = drawerConfig;
-      this.drawers = drawers;
-      this.scheduleUpdate();
-    } else {
+    if (!oldDrawerConfig) {
       throw new Error(`[AwsUi] [runtime drawers] drawer with id ${drawerId} not found`);
     }
+    const drawers = this.drawers.slice();
+    const updatedDrawer = { ...oldDrawerConfig };
+    for (const key of updatableProperties) {
+      if (key in rest) {
+        updatedDrawer[key] = (rest as any)[key];
+      }
+    }
+    drawers[drawerIndex] = updatedDrawer;
+    this.drawers = drawers;
+    this.scheduleUpdate();
   };
 
   onDrawersRegistered = (listener: DrawersRegistrationListener) => {