diff --git a/packages/@react-aria/autocomplete/src/useAutocomplete.ts b/packages/@react-aria/autocomplete/src/useAutocomplete.ts
index 9ff0d4fd2b0..40eee24ae05 100644
--- a/packages/@react-aria/autocomplete/src/useAutocomplete.ts
+++ b/packages/@react-aria/autocomplete/src/useAutocomplete.ts
@@ -18,7 +18,7 @@ import {dispatchVirtualBlur, dispatchVirtualFocus, getVirtuallyFocusedElement, m
 import {getInteractionModality, getPointerType} from '@react-aria/interactions';
 // @ts-ignore
 import intlMessages from '../intl/*.json';
-import {FocusEvent as ReactFocusEvent, KeyboardEvent as ReactKeyboardEvent, useCallback, useEffect, useMemo, useRef, useState} from 'react';
+import {FocusEvent as ReactFocusEvent, KeyboardEvent as ReactKeyboardEvent, PointerEvent as ReactPointerEvent, useCallback, useEffect, useMemo, useRef, useState} from 'react';
 import {useLocalizedStringFormatter} from '@react-aria/i18n';
 
 export interface CollectionOptions extends DOMProps, AriaLabelingProps {
@@ -420,6 +420,20 @@ export function useAutocomplete<T>(props: AriaAutocompleteOptions<T>, state: Aut
     }
   };
 
+  // Clicking back into the input can happen after focus moved elsewhere in the dialog, while
+  // virtual focus is still on an option. Clear virtual focus on pointer down so mouse
+  // interactions restore the input state before the click's focus handling runs.
+  // Touch is excluded because touch interactions should not move focus back to the input.
+  let onPointerDown = (e: ReactPointerEvent) => {
+    if (e.button !== 0 || e.pointerType === 'touch' || queuedActiveDescendant.current == null || inputRef.current == null) {
+      return;
+    }
+
+    if (getEventTarget(e) === inputRef.current) {
+      clearVirtualFocus();
+    }
+  };
+
   // Only apply the autocomplete specific behaviors if the collection component wrapped by it is actually
   // being filtered/allows filtering by the Autocomplete.
   let inputProps = {
@@ -431,7 +445,8 @@ export function useAutocomplete<T>(props: AriaAutocompleteOptions<T>, state: Aut
     onKeyDown,
     'aria-activedescendant': state.focusedNodeId ?? undefined,
     onBlur,
-    onFocus
+    onFocus,
+    onPointerDown
   };
 
   if (hasCollection) {
diff --git a/packages/react-aria-components/stories/Autocomplete.stories.tsx b/packages/react-aria-components/stories/Autocomplete.stories.tsx
index 5bc6de445fe..b2368147ff9 100644
--- a/packages/react-aria-components/stories/Autocomplete.stories.tsx
+++ b/packages/react-aria-components/stories/Autocomplete.stories.tsx
@@ -166,6 +166,29 @@ export const AutocompleteSearchfield: AutocompleteStory = {
   }
 };
 
+export const AutocompleteFocusRecovery: AutocompleteStory = {
+  render: (args) => {
+    return (
+      <AutocompleteWrapper disableVirtualFocus={args.disableVirtualFocus}>
+        <div>
+          <TextField autoFocus data-testid="autocomplete-focus-recovery">
+            <Label style={{display: 'block'}}>Test</Label>
+            <Input />
+            <Text style={{display: 'block'}} slot="description">Focus the input, move virtual focus to an option, then click the input again.</Text>
+          </TextField>
+          <StaticMenu {...args} />
+        </div>
+      </AutocompleteWrapper>
+    );
+  },
+  name: 'Autocomplete focus recovery after virtual focus',
+  parameters: {
+    description: {
+      data: 'Manual check: focus the input, hover or keyboard navigate to an option, then click the input again. The input should regain focused styling and the active descendant should clear.'
+    }
+  }
+};
+
 // Note that the trigger items in this array MUST have an id, even if the underlying MenuItem might apply its own
 // id. If it is omitted, we can't build the collection node for the trigger node and an error will throw
 let dynamicAutocompleteSubdialog: MenuNode[] = [
diff --git a/packages/react-aria-components/test/Autocomplete.test.tsx b/packages/react-aria-components/test/Autocomplete.test.tsx
index e30cee9a5f1..d935a8e61da 100644
--- a/packages/react-aria-components/test/Autocomplete.test.tsx
+++ b/packages/react-aria-components/test/Autocomplete.test.tsx
@@ -496,6 +496,100 @@ describe('Autocomplete', () => {
     expect(input).toHaveAttribute('data-focus-visible');
   });
 
+  it('should restore focused styles to the input when clicking it after hovering an option', async () => {
+    let {getByRole} = render(
+      <AutocompleteWrapper>
+        <StaticMenu />
+      </AutocompleteWrapper>
+    );
+
+    let input = getByRole('searchbox');
+    await user.click(input);
+    expect(document.activeElement).toBe(input);
+    expect(input).toHaveAttribute('data-focused');
+
+    let menu = getByRole('menu');
+    let options = within(menu).getAllByRole('menuitem');
+    await user.hover(options[1]);
+
+    expect(options[1]).toHaveAttribute('data-focused');
+    expect(input).not.toHaveAttribute('data-focused');
+    expect(input).toHaveAttribute('aria-activedescendant', options[1].id);
+
+    await user.click(input);
+
+    expect(document.activeElement).toBe(input);
+    expect(input).toHaveAttribute('data-focused');
+    expect(input).not.toHaveAttribute('data-focus-visible');
+    expect(input).not.toHaveAttribute('aria-activedescendant');
+    expect(options[1]).not.toHaveAttribute('data-focused');
+  });
+
+  it('should restore the input state after clicking outside the autocomplete and then back into the input', async () => {
+    let {getByRole} = render(
+      <>
+        <button type="button">Outside</button>
+        <AutocompleteWrapper>
+          <StaticMenu />
+        </AutocompleteWrapper>
+      </>
+    );
+
+    let input = getByRole('searchbox');
+    await user.click(input);
+
+    let menu = getByRole('menu');
+    let options = within(menu).getAllByRole('menuitem');
+    await user.hover(options[1]);
+
+    expect(input).toHaveAttribute('aria-activedescendant', options[1].id);
+    expect(options[1]).toHaveAttribute('data-focused');
+
+    await user.click(getByRole('button', {name: 'Outside'}));
+    expect(document.activeElement).toHaveTextContent('Outside');
+    expect(input).not.toHaveAttribute('data-focused');
+    expect(input).not.toHaveAttribute('data-focus-visible');
+
+    await user.click(input);
+
+    expect(document.activeElement).toBe(input);
+    expect(input).toHaveAttribute('data-focused');
+    expect(input).not.toHaveAttribute('data-focus-visible');
+    expect(input).not.toHaveAttribute('aria-activedescendant');
+    expect(options[1]).not.toHaveAttribute('data-focused');
+  });
+
+  it('should restore focused styles to the input when clicking it after keyboard focusing an option', async () => {
+    let {getByRole} = render(
+      <AutocompleteWrapper>
+        <StaticMenu />
+      </AutocompleteWrapper>
+    );
+
+    let input = getByRole('searchbox');
+    await user.click(input);
+    expect(document.activeElement).toBe(input);
+
+    await user.keyboard('{ArrowDown}');
+    act(() => jest.runAllTimers());
+
+    let menu = getByRole('menu');
+    let options = within(menu).getAllByRole('menuitem');
+    expect(options[0]).toHaveAttribute('data-focus-visible');
+    expect(input).not.toHaveAttribute('data-focused');
+    expect(input).toHaveAttribute('aria-activedescendant', options[0].id);
+
+    await user.click(input);
+    act(() => jest.runAllTimers());
+
+    expect(document.activeElement).toBe(input);
+    expect(input).toHaveAttribute('data-focused');
+    expect(input).not.toHaveAttribute('data-focus-visible');
+    expect(input).not.toHaveAttribute('aria-activedescendant');
+    expect(options[0]).not.toHaveAttribute('data-focused');
+    expect(options[0]).not.toHaveAttribute('data-focus-visible');
+  });
+
   it('should not display focus in the virtually focused menu if focus isn\'t in the autocomplete input', async function () {
     let {getByRole} = render(
       <>
diff --git a/starters/docs/src/TextField.css b/starters/docs/src/TextField.css
index cd613396730..2fbcd5ca075 100644
--- a/starters/docs/src/TextField.css
+++ b/starters/docs/src/TextField.css
@@ -24,7 +24,7 @@
     color: var(--text-color-placeholder);
   }
 
-  &[data-focused] {
+  &[data-focus-visible] {
     outline: 2px solid var(--focus-ring-color);
     outline-offset: -1px;
   }