diff --git a/packages/@react-aria/autocomplete/src/useAutocomplete.ts b/packages/@react-aria/autocomplete/src/useAutocomplete.ts
index 3126f1ce9b6..24abb0f0fbb 100644
--- a/packages/@react-aria/autocomplete/src/useAutocomplete.ts
+++ b/packages/@react-aria/autocomplete/src/useAutocomplete.ts
@@ -32,7 +32,13 @@ export interface AriaAutocompleteProps extends AutocompleteProps {
    * An optional filter function used to determine if a option should be included in the autocomplete list.
    * Include this if the items you are providing to your wrapped collection aren't filtered by default.
    */
-  filter?: (textValue: string, inputValue: string) => boolean
+  filter?: (textValue: string, inputValue: string) => boolean,
+
+  /**
+   * Whether or not to focus the first item in the collection after a filter is performed.
+   * @default false
+   */
+  disableAutoFocusFirst?: boolean
 }
 
 export interface AriaAutocompleteOptions extends Omit<AriaAutocompleteProps, 'children'> {
@@ -63,7 +69,8 @@ export function useAutocomplete(props: AriaAutocompleteOptions, state: Autocompl
   let {
     inputRef,
     collectionRef,
-    filter
+    filter,
+    disableAutoFocusFirst = false
   } = props;
 
   let collectionId = useId();
@@ -160,7 +167,7 @@ export function useAutocomplete(props: AriaAutocompleteOptions, state: Autocompl
   let onChange = (value: string) => {
     // Tell wrapped collection to focus the first element in the list when typing forward and to clear focused key when deleting text
     // for screen reader announcements
-    if (state.inputValue !== value && state.inputValue.length <= value.length) {
+    if (state.inputValue !== value && state.inputValue.length <= value.length && !disableAutoFocusFirst) {
       focusFirstItem();
     } else {
       // Fully clear focused key when backspacing since the list may change and thus we'd want to start fresh again
diff --git a/packages/react-aria-components/src/Autocomplete.tsx b/packages/react-aria-components/src/Autocomplete.tsx
index f8096393c80..49478f06a33 100644
--- a/packages/react-aria-components/src/Autocomplete.tsx
+++ b/packages/react-aria-components/src/Autocomplete.tsx
@@ -39,7 +39,7 @@ export const UNSTABLE_InternalAutocompleteContext = createContext<InternalAutoco
 export function Autocomplete(props: AutocompleteProps) {
   let ctx = useSlottedContext(AutocompleteContext, props.slot);
   props = mergeProps(ctx, props);
-  let {filter} = props;
+  let {filter, disableAutoFocusFirst} = props;
   let state = useAutocompleteState(props);
   let inputRef = useRef<HTMLInputElement | null>(null);
   let collectionRef = useRef<HTMLElement>(null);
@@ -51,6 +51,7 @@ export function Autocomplete(props: AutocompleteProps) {
   } = useAutocomplete({
     ...removeDataAttributes(props),
     filter,
+    disableAutoFocusFirst,
     inputRef,
     collectionRef
   }, state);
diff --git a/packages/react-aria-components/test/Autocomplete.test.tsx b/packages/react-aria-components/test/Autocomplete.test.tsx
index a7b49d89e72..79a7aa5cebe 100644
--- a/packages/react-aria-components/test/Autocomplete.test.tsx
+++ b/packages/react-aria-components/test/Autocomplete.test.tsx
@@ -610,6 +610,27 @@ describe('Autocomplete', () => {
 
     expect(document.activeElement).toBe(secondButton);
   });
+
+  it('should not auto focus first item when disableAutoFocusFirst is true', async () => {
+    let {getByRole} = render(
+      <AutocompleteWrapper autocompleteProps={{disableAutoFocusFirst: true}}>
+        <StaticMenu />
+      </AutocompleteWrapper>
+    );
+
+    let input = getByRole('searchbox');
+    await user.tab();
+    expect(document.activeElement).toBe(input);
+
+    await user.keyboard('Foo');
+
+    expect(input).not.toHaveAttribute('aria-activedescendant');
+
+    await user.keyboard('{ArrowDown}');
+    let menu = getByRole('menu');
+    let options = within(menu).getAllByRole('menuitem');
+    expect(input).toHaveAttribute('aria-activedescendant', options[0].id);
+  });
 });
 
 AriaAutocompleteTests({