diff --git a/packages/react-aria-components/test/ComboBox.test.js b/packages/react-aria-components/test/ComboBox.test.js
index 93145bacfed..92dc68e5e07 100644
--- a/packages/react-aria-components/test/ComboBox.test.js
+++ b/packages/react-aria-components/test/ComboBox.test.js
@@ -24,6 +24,7 @@ import {ListLayout} from 'react-stately/private/layout/ListLayout';
 import {Popover} from '../src/Popover';
 import React, {useState} from 'react';
 import {Text} from '../src/Text';
+import {useAsyncList} from 'react-stately/useAsyncList';
 import {User} from '@react-aria/test-utils';
 import userEvent from '@testing-library/user-event';
 import {Virtualizer} from '../src/Virtualizer';
@@ -857,11 +858,11 @@ describe('ComboBox', () => {
     act(() => {getByTestId('form').checkValidity();});
     expect(combobox).toHaveAttribute('aria-describedby');
     expect(container.querySelector('.react-aria-ComboBox')).toHaveAttribute('data-invalid');
-    
+
     await comboboxTester.open();
     let options = comboboxTester.options();
     await user.click(options[0]);
-    
+
     act(() => combobox.blur());
     expect(combobox).not.toHaveAttribute('required');
     expect(combobox.validity.valid).toBe(true);
@@ -937,4 +938,199 @@ describe('ComboBox', () => {
     expect(comboboxTester.combobox).toHaveFocus();
     expect(onOpenChange).toHaveBeenCalledTimes(1);
   });
+
+  it('should re-open the menu when controlled items go from empty to non-empty controlled items', async () => {
+    let onOpenChange = jest.fn();
+    let onInputChange = jest.fn().mockReturnValueOnce(true).mockReturnValue(false);
+
+    function ControlledComboBox() {
+      let [items, setItems] = useState([{id: 1, name: 'Luke Skywalker'}]);
+      return (
+        <ComboBox
+          items={items}
+          onInputChange={() => {
+            if (onInputChange()) {
+              setItems([]);
+            } else {
+              setItems([{id: 1, name: 'Luke Skywalker'}]);
+            }
+          }}
+          onOpenChange={onOpenChange}>
+          <Label>SW Characters</Label>
+          <Input />
+          <Button>{'<'}</Button>
+          <Popover>
+            <ListBox>
+              {(item) => {
+                return <ListBoxItem id={item.id}>{item.name}</ListBoxItem>;
+              }}
+            </ListBox>
+          </Popover>
+        </ComboBox>
+      );
+    }
+
+    let {container, queryByRole} = render(<ControlledComboBox />);
+    let comboboxTester = testUtilUser.createTester('ComboBox', {root: container});
+    await user.tab();
+    await user.keyboard('{ArrowDown}');
+    expect(onOpenChange).toHaveBeenCalledTimes(1);
+    expect(comboboxTester.listbox).toBeVisible();
+    onOpenChange.mockClear();
+
+    await user.keyboard('L');
+    expect(queryByRole('listbox')).toBeNull();
+
+    await user.keyboard('{Backspace}');
+    expect(comboboxTester.listbox).toBeVisible();
+  });
+
+  it('should re-open the menu with useAsyncList after an empty async result then backspace', async () => {
+    const ASYNC_DELAY_MS = 50;
+
+    function itemsForFilterText(filterText) {
+      if (filterText === 'luka') {
+        return [];
+      }
+      return [{id: 1, name: 'Luke Skywalker'}];
+    }
+
+    function AsyncComboBox() {
+      let list = useAsyncList({
+        getKey: (item) => item.id,
+        async load({filterText}) {
+          let rows = itemsForFilterText(filterText);
+          await new Promise((resolve) => setTimeout(resolve, ASYNC_DELAY_MS));
+          return {items: rows};
+        }
+      });
+
+      return (
+        <ComboBox items={list.items} inputValue={list.filterText} onInputChange={list.setFilterText}>
+          <Label>SW Characters</Label>
+          <Input />
+          <Button>{'<'}</Button>
+          <Popover>
+            <ListBox>
+              {(item) => <ListBoxItem id={item.id}>{item.name}</ListBoxItem>}
+            </ListBox>
+          </Popover>
+        </ComboBox>
+      );
+    }
+
+    let {container, queryByRole} = render(<AsyncComboBox />);
+    let comboboxTester = testUtilUser.createTester('ComboBox', {root: container});
+
+    await act(async () => {
+      jest.runAllTimers();
+    });
+
+    await user.tab();
+    await user.keyboard('{ArrowDown}');
+    await act(async () => {
+      jest.runAllTimers();
+    });
+    expect(comboboxTester.listbox).toBeVisible();
+    expect(
+      within(comboboxTester.listbox).getByRole('option', {name: 'Luke Skywalker'})
+    ).toBeInTheDocument();
+
+    await user.keyboard('luka');
+    await act(async () => {
+      jest.runAllTimers();
+    });
+    expect(queryByRole('listbox')).toBeNull();
+
+    await user.keyboard('{Backspace}');
+    expect(queryByRole('listbox')).toBeNull();
+    await act(async () => {
+      jest.runAllTimers();
+    });
+    expect(comboboxTester.listbox).toBeVisible();
+    expect(
+      within(comboboxTester.listbox).getByRole('option', {name: 'Luke Skywalker'})
+    ).toBeInTheDocument();
+  });
+
+  it('should still close the menu when uncontrolled items are empty', async () => {
+    let onOpenChange = jest.fn();
+
+    let items = [{id: 1, name: 'Luke Skywalker'}];
+    function ControlledComboBox() {
+      return (
+        <ComboBox
+          defaultItems={items}
+          onOpenChange={onOpenChange}>
+          <Label>SW Characters</Label>
+          <Input />
+          <Button>{'<'}</Button>
+          <Popover>
+            <ListBox>
+              {(item) => {
+                return <ListBoxItem id={item.id}>{item.name}</ListBoxItem>;
+              }}
+            </ListBox>
+          </Popover>
+        </ComboBox>
+      );
+    }
+
+    let {container, queryByRole} = render(<ControlledComboBox />);
+    let comboboxTester = testUtilUser.createTester('ComboBox', {root: container});
+    await user.tab();
+    await user.keyboard('{ArrowDown}');
+    expect(onOpenChange).toHaveBeenCalledTimes(1);
+    expect(comboboxTester.listbox).toBeVisible();
+    onOpenChange.mockClear();
+
+    await user.keyboard('Z');
+    expect(queryByRole('listbox')).toBeNull();
+  });
+
+  it('should not re-open after user dismisses with Escape (revert) controlled items', async () => {
+    let onOpenChange = jest.fn();
+    let onInputChange = jest.fn().mockReturnValueOnce(true).mockReturnValue(false);
+
+    function ControlledComboBox() {
+      let [items, setItems] = useState([{id: 1, name: 'Luke Skywalker'}]);
+      return (
+        <ComboBox
+          items={items}
+          onInputChange={() => {
+            if (onInputChange()) {
+              setItems([]);
+            } else {
+              setItems([{id: 1, name: 'Luke Skywalker'}]);
+            }
+          }}
+          onOpenChange={onOpenChange}>
+          <Label>SW Characters</Label>
+          <Input />
+          <Button>{'<'}</Button>
+          <Popover>
+            <ListBox>
+              {(item) => {
+                return <ListBoxItem id={item.id}>{item.name}</ListBoxItem>;
+              }}
+            </ListBox>
+          </Popover>
+        </ComboBox>
+      );
+    }
+
+    let {container, queryByRole} = render(<ControlledComboBox />);
+    let comboboxTester = testUtilUser.createTester('ComboBox', {root: container});
+    await user.tab();
+    await user.keyboard('{ArrowDown}');
+    expect(onOpenChange).toHaveBeenCalledTimes(1);
+    expect(comboboxTester.listbox).toBeVisible();
+    onOpenChange.mockClear();
+
+    await user.keyboard('L');
+    expect(queryByRole('listbox')).toBeNull();
+
+    await user.keyboard('{Escape}');
+    expect(queryByRole('listbox')).toBeNull();
+  });
 });
diff --git a/packages/react-stately/src/combobox/useComboBoxState.ts b/packages/react-stately/src/combobox/useComboBoxState.ts
index 02f6bd0116c..8c8ce560b1e 100644
--- a/packages/react-stately/src/combobox/useComboBoxState.ts
+++ b/packages/react-stately/src/combobox/useComboBoxState.ts
@@ -167,6 +167,7 @@ export function useComboBoxState<T extends object, M extends SelectionMode = 'si
   let [showAllItems, setShowAllItems] = useState(false);
   let [isFocused, setFocusedState] = useState(false);
   let [focusStrategy, setFocusStrategy] = useState<FocusStrategy | null>(null);
+  let closedDueToEmptyControlled = useRef(false);
 
   let defaultValue = useMemo(() => {
     return props.defaultValue !== undefined ? props.defaultValue : (selectionMode === 'single' ? props.defaultSelectedKey ?? null : []) as ValueType<M>;
@@ -359,9 +360,25 @@ export function useComboBoxState<T extends object, M extends SelectionMode = 'si
       triggerState.isOpen &&
       filteredCollection.size === 0
     ) {
+      if (props.items != null) {
+        closedDueToEmptyControlled.current = true;
+      }
       closeMenu();
     }
 
+    // Re-open the menu when controlled items become non-empty after being auto-closed due to
+    // an empty collection (e.g. async load completed with results after a previous empty response).
+    if (
+      isFocused &&
+      closedDueToEmptyControlled.current &&
+      filteredCollection.size > 0 &&
+      !triggerState.isOpen &&
+      menuTrigger !== 'manual'
+    ) {
+      closedDueToEmptyControlled.current = false;
+      open(null, 'input');
+    }
+
     // Close when an item is selected.
     if (
       displayValue != null &&
@@ -418,6 +435,7 @@ export function useComboBoxState<T extends object, M extends SelectionMode = 'si
 
   // Revert input value and close menu
   let revert = () => {
+    closedDueToEmptyControlled.current = false;
     if (allowsCustomValue && selectedKey == null) {
       commitCustomValue();
     } else {
@@ -457,6 +475,7 @@ export function useComboBoxState<T extends object, M extends SelectionMode = 'si
   };
 
   const commitValue = () => {
+    closedDueToEmptyControlled.current = false;
     if (allowsCustomValue) {
       const itemText = selectedKey != null ? collection.getItem(selectedKey)?.textValue ?? '' : '';
       (inputValue === itemText) ? commitSelection() : commitCustomValue();
diff --git a/packages/react-stately/test/combobox/useComboBoxState.test.js b/packages/react-stately/test/combobox/useComboBoxState.test.js
index 0f6894144a9..07906d256ec 100644
--- a/packages/react-stately/test/combobox/useComboBoxState.test.js
+++ b/packages/react-stately/test/combobox/useComboBoxState.test.js
@@ -305,4 +305,84 @@ describe('useComboBoxState tests', function () {
       expect(result.current.collection.size).toEqual(2);
     });
   });
+
+  describe('controlled items (async loading)', function () {
+    it('should re-open the menu when controlled items go from empty to non-empty', function () {
+      let onOpenChange = jest.fn();
+      let initialProps = {
+        items: [{id: 1, name: 'Luke Skywalker'}],
+        children: (props) => <Item>{props.name}</Item>,
+        onOpenChange
+      };
+
+      let {result, rerender} = renderHook((props) => useComboBoxState(props), {initialProps});
+
+      // Focus and open the menu by setting input value
+      act(() => {result.current.setFocused(true);});
+      act(() => {result.current.open(null, 'input');});
+      expect(result.current.isOpen).toBe(true);
+
+      // Simulate async load returning empty results (e.g. user typed "luka")
+      rerender({...initialProps, items: []});
+      // Menu closes on empty collection
+      expect(result.current.isOpen).toBe(false);
+
+      // Simulate async load returning results again (e.g. user backspaced to "luk")
+      rerender({...initialProps, items: [{id: 1, name: 'Luke Skywalker'}]});
+      // Menu should re-open because items were controlled and the close was due to empty collection
+      expect(result.current.isOpen).toBe(true);
+      expect(result.current.collection.size).toEqual(1);
+      expect(onOpenChange).toHaveBeenLastCalledWith(true, 'input');
+    });
+
+    it('should not re-open after user dismisses with Escape (revert)', function () {
+      let onOpenChange = jest.fn();
+      let initialProps = {
+        items: [{id: 1, name: 'Luke Skywalker'}],
+        children: (props) => <Item>{props.name}</Item>,
+        onOpenChange
+      };
+
+      let {result, rerender} = renderHook((props) => useComboBoxState(props), {initialProps});
+
+      // Focus and open
+      act(() => {result.current.setFocused(true);});
+      act(() => {result.current.open(null, 'input');});
+      expect(result.current.isOpen).toBe(true);
+
+      // Async returns empty, menu auto-closes
+      rerender({...initialProps, items: []});
+      expect(result.current.isOpen).toBe(false);
+
+      // User presses Escape (revert) while menu is closed
+      act(() => {result.current.revert();});
+
+      // Async returns items — menu should NOT re-open because user explicitly dismissed
+      rerender({...initialProps, items: [{id: 1, name: 'Luke Skywalker'}]});
+      expect(result.current.isOpen).toBe(false);
+    });
+
+    it('should still close the menu when uncontrolled items are empty', function () {
+      let onOpenChange = jest.fn();
+      let contains = (a, b) => a.toLowerCase().includes(b.toLowerCase());
+      let initialProps = {
+        defaultItems: [{id: 1, name: 'Luke Skywalker'}],
+        children: (props) => <Item>{props.name}</Item>,
+        onOpenChange,
+        defaultFilter: contains
+      };
+
+      let {result} = renderHook((props) => useComboBoxState(props), {initialProps});
+
+      // Focus and open
+      act(() => {result.current.setFocused(true);});
+      act(() => {result.current.open(null, 'input');});
+      expect(result.current.isOpen).toBe(true);
+
+      // Type something that filters to zero results
+      act(() => {result.current.setInputValue('zzz');});
+      // Menu should close because items are uncontrolled and filtered to empty
+      expect(result.current.isOpen).toBe(false);
+    });
+  });
 });