diff --git a/packages/@adobe/react-spectrum/test/combobox/ComboBox.test.js b/packages/@adobe/react-spectrum/test/combobox/ComboBox.test.js
index 9c1ea49af91..9d40dd2bfc4 100644
--- a/packages/@adobe/react-spectrum/test/combobox/ComboBox.test.js
+++ b/packages/@adobe/react-spectrum/test/combobox/ComboBox.test.js
@@ -1496,6 +1496,131 @@ describe('ComboBox', function () {
       expect(items).toHaveLength(1);
       expect(combobox).not.toHaveAttribute('aria-activedescendant');
     });
+
+    it("doesn't focus the first item when filtering by default", async function () {
+      let {getByRole} = renderComboBox();
+
+      let combobox = getByRole('combobox');
+      act(() => {
+        combobox.focus();
+      });
+      await user.keyboard('o');
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      let listbox = getByRole('listbox');
+      let items = within(listbox).getAllByRole('option');
+      expect(items).toHaveLength(2);
+      expect(combobox).not.toHaveAttribute('aria-activedescendant');
+    });
+
+    it('focuses the first item when filtering if autoFocusFirst is true', async function () {
+      let {getByRole} = renderComboBox({autoFocusFirst: true});
+
+      let combobox = getByRole('combobox');
+      act(() => {
+        combobox.focus();
+      });
+      await user.keyboard('o');
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      let listbox = getByRole('listbox');
+      let items = within(listbox).getAllByRole('option');
+      expect(items).toHaveLength(2);
+      expect(items[0]).toHaveTextContent('One');
+      expect(combobox).toHaveAttribute('aria-activedescendant', items[0].id);
+
+      // Narrowing the filter further should keep moving focus to the new first match.
+      await user.keyboard('ne');
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      items = within(listbox).getAllByRole('option');
+      expect(items).toHaveLength(1);
+      expect(items[0]).toHaveTextContent('One');
+      expect(combobox).toHaveAttribute('aria-activedescendant', items[0].id);
+    });
+
+    it('still focuses the first item if the menu was already open before typing', async function () {
+      let {getByRole} = renderComboBox({autoFocusFirst: true});
+
+      let button = getByRole('button');
+      await user.click(button);
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      let combobox = getByRole('combobox');
+      let listbox = getByRole('listbox');
+      await user.keyboard('o');
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      let items = within(listbox).getAllByRole('option');
+      expect(combobox).toHaveAttribute('aria-activedescendant', items[0].id);
+    });
+
+    it('does not get stuck on a stale selection when re-searching after selecting an item', async function () {
+      let {getByRole} = renderComboBox({autoFocusFirst: true});
+
+      let combobox = getByRole('combobox');
+      act(() => {
+        combobox.focus();
+      });
+      await user.keyboard('One');
+      act(() => {
+        jest.runAllTimers();
+      });
+      await user.keyboard('[Enter]');
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      await user.clear(combobox);
+      await user.keyboard('T');
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      let listbox = getByRole('listbox');
+      let items = within(listbox).getAllByRole('option');
+      expect(items[0]).toHaveTextContent('Two');
+      expect(combobox).toHaveAttribute('aria-activedescendant', items[0].id);
+    });
+
+    it('clears the focused option when the input is cleared back to empty', async function () {
+      let {getByRole} = renderComboBox({autoFocusFirst: true});
+
+      let combobox = getByRole('combobox');
+      act(() => {
+        combobox.focus();
+      });
+      await user.keyboard('One');
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      let listbox = getByRole('listbox');
+      let items = within(listbox).getAllByRole('option');
+      expect(combobox).toHaveAttribute('aria-activedescendant', items[0].id);
+
+      await user.clear(combobox);
+      act(() => {
+        jest.runAllTimers();
+      });
+
+      // Clearing returns to the unfiltered list, which should not be treated as "a filter was
+      // performed," so no option should be focused until the user navigates explicitly.
+      listbox = getByRole('listbox');
+      items = within(listbox).getAllByRole('option');
+      expect(items).toHaveLength(3);
+      expect(combobox).not.toHaveAttribute('aria-activedescendant');
+    });
   });
 
   describe('blur', function () {
diff --git a/packages/react-stately/src/combobox/useComboBoxState.ts b/packages/react-stately/src/combobox/useComboBoxState.ts
index af0d29deded..6b829845ce0 100644
--- a/packages/react-stately/src/combobox/useComboBoxState.ts
+++ b/packages/react-stately/src/combobox/useComboBoxState.ts
@@ -115,6 +115,13 @@ export interface ComboBoxProps<T, M extends SelectionMode = 'single'>
    * @default 'input'
    */
   menuTrigger?: MenuTriggerAction;
+  /**
+   * Whether to automatically focus the first item in the ComboBox's listbox when the
+   * user filters the list by typing into the input.
+   *
+   * @default false
+   */
+  autoFocusFirst?: boolean;
 }
 
 export interface ComboBoxState<T, M extends SelectionMode = 'single'>
@@ -200,7 +207,8 @@ export function useComboBoxState<T, M extends SelectionMode = 'single'>(
     allowsEmptyCollection = false,
     allowsCustomValue,
     shouldCloseOnBlur = true,
-    selectionMode = 'single' as SelectionMode
+    selectionMode = 'single' as SelectionMode,
+    autoFocusFirst = false
   } = props;
 
   let [showAllItems, setShowAllItems] = useState(false);
@@ -409,6 +417,7 @@ export function useComboBoxState<T, M extends SelectionMode = 'single'>(
   let lastSelectedKeyText = useRef(
     selectedKey != null ? (collection.getItem(selectedKey)?.textValue ?? '') : ''
   );
+  let shouldAutoFocusFirst = autoFocusFirst && inputValue !== '';
   // intentional omit dependency array, want this to happen on every render
   // eslint-disable-next-line react-hooks/exhaustive-deps
   useEffect(() => {
@@ -422,7 +431,7 @@ export function useComboBoxState<T, M extends SelectionMode = 'single'>(
       menuTrigger !== 'manual'
     ) {
       // oxlint-disable-next-line react/react-compiler
-      open(null, 'input');
+      open(shouldAutoFocusFirst ? 'first' : null, 'input');
     }
 
     // Close the menu if the collection is empty. Don't close menu if filtered collection size is 0
@@ -447,7 +456,9 @@ export function useComboBoxState<T, M extends SelectionMode = 'single'>(
 
     // Clear focused key when input value changes and display filtered collection again.
     if (inputValue !== lastValue) {
-      selectionManager.setFocusedKey(null);
+      selectionManager.setFocusedKey(
+        shouldAutoFocusFirst ? filteredCollection.getFirstKey() : null
+      );
       setShowAllItems(false);
 
       // Set value to null when the user clears the input.