diff --git a/packages/@react-aria/interactions/src/useInteractOutside.ts b/packages/@react-aria/interactions/src/useInteractOutside.ts
index 3a63ada5297..5bc6cd69f7d 100644
--- a/packages/@react-aria/interactions/src/useInteractOutside.ts
+++ b/packages/@react-aria/interactions/src/useInteractOutside.ts
@@ -20,6 +20,7 @@ import {RefObject, SyntheticEvent, useEffect, useRef} from 'react';
 interface InteractOutsideProps {
   ref: RefObject<Element>,
   onInteractOutside?: (e: SyntheticEvent) => void,
+  onInteractOutsideStart?: (e: SyntheticEvent) => void,
   /** Whether the interact outside events should be disabled. */
   isDisabled?: boolean
 }
@@ -29,7 +30,7 @@ interface InteractOutsideProps {
  * when a user clicks outside them.
  */
 export function useInteractOutside(props: InteractOutsideProps) {
-  let {ref, onInteractOutside, isDisabled} = props;
+  let {ref, onInteractOutside, isDisabled, onInteractOutsideStart} = props;
   let stateRef = useRef({
     isPointerDown: false,
     ignoreEmulatedMouseEvents: false
@@ -41,7 +42,10 @@ export function useInteractOutside(props: InteractOutsideProps) {
       if (isDisabled) {
         return;
       }
-      if (isValidEvent(e, ref)) {
+      if (isValidEvent(e, ref) && onInteractOutside) {
+        if (onInteractOutsideStart) {
+          onInteractOutsideStart(e);
+        }
         state.isPointerDown = true;
       }
     };
diff --git a/packages/@react-aria/menu/stories/useMenu.stories.tsx b/packages/@react-aria/menu/stories/useMenu.stories.tsx
index b35e8d58055..29f3505ec70 100644
--- a/packages/@react-aria/menu/stories/useMenu.stories.tsx
+++ b/packages/@react-aria/menu/stories/useMenu.stories.tsx
@@ -28,7 +28,7 @@ storiesOf('useMenu', module)
   .add('double menu fires onInteractOutside',
     () => (
       <div>
-        <div>This should just be there to show that onInteractOutside fires when clicking on another trigger, don't worry about two open menus at once.</div>
+        <div>This should just be there to show that onInteractOutside fires when clicking on another trigger.</div>
         <MenuButton label="Actions">
           <Item key="copy">Copy</Item>
           <Item key="cut">Cut</Item>
@@ -39,6 +39,7 @@ storiesOf('useMenu', module)
           <Item key="cut">Cut</Item>
           <Item key="paste">Paste</Item>
         </MenuButton>
+        <input />
       </div>
     )
   );
diff --git a/packages/@react-aria/overlays/src/useOverlay.ts b/packages/@react-aria/overlays/src/useOverlay.ts
index 991af37381d..b987345193e 100644
--- a/packages/@react-aria/overlays/src/useOverlay.ts
+++ b/packages/@react-aria/overlays/src/useOverlay.ts
@@ -89,8 +89,21 @@ export function useOverlay(props: OverlayProps, ref: RefObject<HTMLElement>): Ov
     }
   };
 
+  let onInteractOutsideStart = (e: SyntheticEvent<HTMLElement>) => {
+    if (!shouldCloseOnInteractOutside || shouldCloseOnInteractOutside(e.target as HTMLElement)) {
+      if (visibleOverlays[visibleOverlays.length - 1] === ref) {
+        e.stopPropagation();
+        e.preventDefault();
+      }
+    }
+  };
+
   let onInteractOutside = (e: SyntheticEvent<HTMLElement>) => {
     if (!shouldCloseOnInteractOutside || shouldCloseOnInteractOutside(e.target as HTMLElement)) {
+      if (visibleOverlays[visibleOverlays.length - 1] === ref) {
+        e.stopPropagation();
+        e.preventDefault();
+      }
       onHide();
     }
   };
@@ -104,7 +117,7 @@ export function useOverlay(props: OverlayProps, ref: RefObject<HTMLElement>): Ov
   };
 
   // Handle clicking outside the overlay to close it
-  useInteractOutside({ref, onInteractOutside: isDismissable ? onInteractOutside : null});
+  useInteractOutside({ref, onInteractOutside: isDismissable ? onInteractOutside : null, onInteractOutsideStart});
 
   let {focusWithinProps} = useFocusWithin({
     isDisabled: !shouldCloseOnBlur,
diff --git a/packages/@react-spectrum/breadcrumbs/test/Breadcrumbs.test.js b/packages/@react-spectrum/breadcrumbs/test/Breadcrumbs.test.js
index 1742ddafe07..2776b91e440 100644
--- a/packages/@react-spectrum/breadcrumbs/test/Breadcrumbs.test.js
+++ b/packages/@react-spectrum/breadcrumbs/test/Breadcrumbs.test.js
@@ -10,15 +10,18 @@
  * governing permissions and limitations under the License.
  */
 
+import {act, render, within} from '@testing-library/react';
 import {Breadcrumbs} from '../';
 import {Item} from '@react-stately/collections';
 import {Provider} from '@react-spectrum/provider';
 import React, {useRef} from 'react';
-import {render, within} from '@testing-library/react';
 import {theme} from '@react-spectrum/theme-default';
 import {triggerPress} from '@react-spectrum/test-utils';
 
 describe('Breadcrumbs', function () {
+  beforeAll(() => {
+    jest.useFakeTimers();
+  });
   beforeEach(() => {
     jest.spyOn(HTMLElement.prototype, 'offsetWidth', 'get').mockImplementation(function () {
       if (this instanceof HTMLUListElement) {
@@ -299,6 +302,7 @@ describe('Breadcrumbs', function () {
 
     let menuButton = getByRole('button');
     triggerPress(menuButton);
+    act(() => {jest.runAllTimers();});
 
     let menu = getByRole('menu');
     expect(menu).toBeTruthy();
@@ -311,6 +315,9 @@ describe('Breadcrumbs', function () {
     // breadcrumb root item
     expect(item1[0]).toHaveAttribute('role', 'link');
     triggerPress(item1[0]);
+    // first press closes the menu, second press
+    act(() => {jest.runAllTimers();});
+    triggerPress(item1[0]);
     expect(onAction).toHaveBeenCalledWith('Folder 1');
 
     // menu item
diff --git a/packages/@react-spectrum/combobox/src/ComboBox.tsx b/packages/@react-spectrum/combobox/src/ComboBox.tsx
index 8ba2eeef19f..9f2088a1181 100644
--- a/packages/@react-spectrum/combobox/src/ComboBox.tsx
+++ b/packages/@react-spectrum/combobox/src/ComboBox.tsx
@@ -162,7 +162,8 @@ const ComboBoxBase = React.forwardRef(function ComboBoxBase<T extends object>(pr
         ref={popoverRef}
         placement={placement}
         hideArrow
-        isNonModal>
+        isNonModal
+        isDismissable={false}>
         <ListBoxBase
           ref={listBoxRef}
           domProps={listBoxProps}
diff --git a/packages/@react-spectrum/combobox/stories/ComboBox.stories.tsx b/packages/@react-spectrum/combobox/stories/ComboBox.stories.tsx
index c13efdfaf8c..b0e4460016e 100644
--- a/packages/@react-spectrum/combobox/stories/ComboBox.stories.tsx
+++ b/packages/@react-spectrum/combobox/stories/ComboBox.stories.tsx
@@ -454,6 +454,19 @@ storiesOf('ComboBox', module)
     () => (
       <AsyncLoadingExampleControlledKeyWithReset />
     )
+  )
+  .add(
+    '2 comboboxes',
+    () => (
+      <Flex gap="size-100">
+        <ComboBox defaultItems={items} label="Combobox1">
+          {(item) => <Item>{item.name}</Item>}
+        </ComboBox>
+        <ComboBox defaultItems={items} label="Combobox2">
+          {(item) => <Item>{item.name}</Item>}
+        </ComboBox>
+      </Flex>
+    )
   );
 
 
diff --git a/packages/@react-spectrum/combobox/test/ComboBox.test.js b/packages/@react-spectrum/combobox/test/ComboBox.test.js
index 60a49abc6c0..3a8fad61293 100644
--- a/packages/@react-spectrum/combobox/test/ComboBox.test.js
+++ b/packages/@react-spectrum/combobox/test/ComboBox.test.js
@@ -424,6 +424,22 @@ describe('ComboBox', function () {
         expect(onOpenChange).toHaveBeenCalledWith(true, 'focus');
         testComboBoxOpen(combobox, button, listbox);
       });
+
+      it('opens menu when combobox is focused by clicking button', function () {
+        let {getByRole} = renderComboBox({menuTrigger: 'focus'});
+
+        let button = getByRole('button');
+        let combobox = getByRole('combobox');
+        act(() => {
+          triggerPress(button);
+          jest.runAllTimers();
+        });
+
+        let listbox = getByRole('listbox');
+        expect(onOpenChange).toBeCalledTimes(1);
+        expect(onOpenChange).toHaveBeenCalledWith(true, 'focus');
+        testComboBoxOpen(combobox, button, listbox);
+      });
     });
 
     describe('button click', function () {
diff --git a/packages/@react-spectrum/dialog/stories/DialogTrigger.stories.tsx b/packages/@react-spectrum/dialog/stories/DialogTrigger.stories.tsx
index 3f0f94c121c..88be1688a33 100644
--- a/packages/@react-spectrum/dialog/stories/DialogTrigger.stories.tsx
+++ b/packages/@react-spectrum/dialog/stories/DialogTrigger.stories.tsx
@@ -335,6 +335,26 @@ storiesOf('DialogTrigger', module)
   .add(
     'trigger visible through underlay',
     () => renderTriggerNotCentered({})
+  )
+  .add(
+    '2 popovers',
+    () => (
+      <Flex gap="size-200">
+        <DialogTrigger type="popover">
+          <ActionButton>Trigger</ActionButton>
+          <Dialog>
+            <Content>
+              <input />
+              <input />
+            </Content>
+          </Dialog>
+        </DialogTrigger>
+        <DialogTrigger type="popover">
+          <ActionButton>Trigger</ActionButton>
+          <Dialog><Content>Hi!</Content></Dialog>
+        </DialogTrigger>
+      </Flex>
+    )
   );
 
 function render({width = 'auto', ...props}) {
diff --git a/packages/@react-spectrum/dialog/test/DialogTrigger.test.js b/packages/@react-spectrum/dialog/test/DialogTrigger.test.js
index 5265e550047..312254ef3ef 100644
--- a/packages/@react-spectrum/dialog/test/DialogTrigger.test.js
+++ b/packages/@react-spectrum/dialog/test/DialogTrigger.test.js
@@ -56,7 +56,7 @@ describe('DialogTrigger', function () {
   });
 
   it('should trigger a modal by default', function () {
-    let {getByRole, getByTestId} = render(
+    let {queryByRole, getByRole, getByTestId} = render(
       <Provider theme={theme}>
         <DialogTrigger>
           <ActionButton>Trigger</ActionButton>
@@ -65,9 +65,7 @@ describe('DialogTrigger', function () {
       </Provider>
     );
 
-    expect(() => {
-      getByRole('dialog');
-    }).toThrow();
+    expect(queryByRole('dialog')).toBeNull();
 
     let button = getByRole('button');
     triggerPress(button);
@@ -323,6 +321,47 @@ describe('DialogTrigger', function () {
     expect(document.activeElement).toBe(button);
   });
 
+  it('popovers should be closeable by clicking their trigger while they are open', async function () {
+    let onOpenChange = jest.fn();
+    let {getByRole} = render(
+      <Provider theme={theme}>
+        <DialogTrigger onOpenChange={onOpenChange} type="popover">
+          <ActionButton>Trigger</ActionButton>
+          <Dialog>contents</Dialog>
+        </DialogTrigger>
+      </Provider>
+    );
+
+    let button = getByRole('button');
+    triggerPress(button);
+
+    act(() => {
+      jest.runAllTimers();
+    });
+
+    let dialog = getByRole('dialog');
+
+    await waitFor(() => {
+      expect(dialog).toBeVisible();
+    }); // wait for animation
+
+    expect(document.activeElement).toBe(dialog);
+    expect(onOpenChange).toHaveBeenCalledTimes(1);
+
+    triggerPress(button);
+
+    act(() => {
+      jest.runAllTimers();
+    });
+
+    await waitFor(() => {
+      expect(dialog).not.toBeInTheDocument();
+    }); // wait for animation
+
+    expect(document.activeElement).toBe(button);
+    expect(onOpenChange).toHaveBeenCalledTimes(2);
+  });
+
   it('should set aria-hidden on parent providers on mount and remove on unmount', async function () {
     let rootProviderRef = React.createRef();
     let {getByRole} = render(
@@ -844,4 +883,60 @@ describe('DialogTrigger', function () {
     });
     expect(document.activeElement).toBe(innerInput);
   });
+
+  it('input in nested popover should be interactive with a click', async () => {
+    let {getByRole, getByText, getByLabelText} = render(
+      <Provider theme={theme}>
+        <TextField id="document-input" aria-label="document input" />
+        <DialogTrigger type="popover">
+          <ActionButton id="outer-trigger">Trigger1</ActionButton>
+          <Dialog id="outer-dialog">
+            <Content>
+              <TextField id="outer-input" aria-label="outer input" />
+              <DialogTrigger type="popover">
+                <ActionButton id="inner-trigger">Trigger2</ActionButton>
+                <Dialog id="inner-dialog">
+                  <Content>
+                    <TextField id="inner-input" label="inner input" />
+                  </Content>
+                </Dialog>
+              </DialogTrigger>
+            </Content>
+          </Dialog>
+        </DialogTrigger>
+      </Provider>
+    );
+    let button = getByRole('button');
+    triggerPress(button);
+
+    act(() => {
+      jest.runAllTimers();
+    });
+
+    let outerDialog = getByRole('dialog');
+
+    await waitFor(() => {
+      expect(outerDialog).toBeVisible();
+    }); // wait for animation
+    let outerButton = getByText('Trigger2');
+
+
+    triggerPress(outerButton);
+
+    act(() => {
+      jest.runAllTimers();
+    });
+
+    let innerDialog = getByRole('dialog');
+
+    await waitFor(() => {
+      expect(innerDialog).toBeVisible();
+    }); // wait for animation
+
+    let innerInput = getByLabelText('inner input');
+    expect(getByLabelText('inner input')).toBeVisible();
+    userEvent.click(innerInput);
+
+    expect(document.activeElement).toBe(innerInput);
+  });
 });
diff --git a/packages/@react-spectrum/menu/test/MenuTrigger.test.js b/packages/@react-spectrum/menu/test/MenuTrigger.test.js
index 76b4945aeae..4aff365a343 100644
--- a/packages/@react-spectrum/menu/test/MenuTrigger.test.js
+++ b/packages/@react-spectrum/menu/test/MenuTrigger.test.js
@@ -211,6 +211,7 @@ describe('MenuTrigger', function () {
     ${'MenuTrigger'} | ${MenuTrigger} | ${{onOpenChange, isOpen: true}}
   `('$Name supports a controlled open state ', function ({Component, props}) {
     let tree = renderComponent(Component, props);
+    act(() => {jest.runAllTimers();});
     expect(onOpenChange).toBeCalledTimes(0);
 
     let menu = tree.getByRole('menu');
@@ -222,7 +223,7 @@ describe('MenuTrigger', function () {
 
     menu = tree.getByRole('menu');
     expect(menu).toBeTruthy();
-    expect(onOpenChange).toBeCalledTimes(2); // once for press, once for blur :/
+    expect(onOpenChange).toBeCalledTimes(1);
   });
 
   // New functionality in v3
@@ -231,6 +232,7 @@ describe('MenuTrigger', function () {
     ${'MenuTrigger'} | ${MenuTrigger} | ${{onOpenChange, defaultOpen: true}}
   `('$Name supports a uncontrolled default open state ', function ({Component, props}) {
     let tree = renderComponent(Component, props);
+    act(() => {jest.runAllTimers();});
     expect(onOpenChange).toBeCalledTimes(0);
 
     let menu = tree.getByRole('menu');
@@ -263,6 +265,7 @@ describe('MenuTrigger', function () {
       ${'MenuTrigger'} | ${MenuTrigger} | ${{}}
     `('$Name autofocuses the selected item on menu open', function ({Component, props}) {
       let tree = renderComponent(Component, props, {selectedKeys: ['Bar']});
+      act(() => {jest.runAllTimers();});
       let button = tree.getByRole('button');
       triggerPress(button);
       act(() => {jest.runAllTimers();});
@@ -278,6 +281,8 @@ describe('MenuTrigger', function () {
 
       // Opening menu via down arrow still autofocuses the selected item
       fireEvent.keyDown(button, {key: 'ArrowDown', code: 40, charCode: 40});
+      fireEvent.keyUp(button, {key: 'ArrowDown', code: 40, charCode: 40});
+      act(() => {jest.runAllTimers();});
       menu = tree.getByRole('menu');
       menuItems = within(menu).getAllByRole('menuitem');
       selectedItem = menuItems[1];
@@ -770,4 +775,48 @@ describe('MenuTrigger', function () {
     let checkmark = queryByRole('img', {hidden: true});
     expect(checkmark).toBeNull();
   });
+
+  it('two menus can not be open at the same time', function () {
+    let {getAllByRole, getByRole, queryByRole} = render(
+      <Provider theme={theme}>
+        <MenuTrigger>
+          <Button>
+            {triggerText}
+          </Button>
+          <Menu items={withSection}>
+            <Item key="alpha">Alpha</Item>
+            <Item key="bravo">Bravo</Item>
+          </Menu>
+        </MenuTrigger>
+        <MenuTrigger>
+          <Button>
+            {triggerText}
+          </Button>
+          <Menu items={withSection}>
+            <Item key="whiskey">Whiskey</Item>
+            <Item key="tango">Tango</Item>
+            <Item key="foxtrot">Foxtrot</Item>
+          </Menu>
+        </MenuTrigger>
+      </Provider>
+    );
+    let [button1, button2] = getAllByRole('button');
+    triggerPress(button1);
+    act(() => jest.runAllTimers());
+    let menu = getByRole('menu');
+    let menuItem1 = within(menu).getByText('Alpha');
+    expect(menuItem1).toBeInTheDocument();
+
+    // pressing once on button 2 should close menu1, but not open menu2 yet
+    triggerPress(button2);
+    act(() => jest.runAllTimers());
+    expect(queryByRole('menu')).toBeNull();
+
+    // second press of button2 should open menu2
+    triggerPress(button2);
+    act(() => jest.runAllTimers());
+    let menu2 = getByRole('menu');
+    let menu2Item1 = within(menu2).getByText('Whiskey');
+    expect(menu2Item1).toBeInTheDocument();
+  });
 });
diff --git a/packages/@react-spectrum/overlays/src/Popover.tsx b/packages/@react-spectrum/overlays/src/Popover.tsx
index ac6a0e8678c..6f6c81c0a5a 100644
--- a/packages/@react-spectrum/overlays/src/Popover.tsx
+++ b/packages/@react-spectrum/overlays/src/Popover.tsx
@@ -29,7 +29,8 @@ interface PopoverWrapperProps extends HTMLAttributes<HTMLElement> {
   onClose?: () => void,
   shouldCloseOnBlur?: boolean,
   isKeyboardDismissDisabled?: boolean,
-  isNonModal?: boolean
+  isNonModal?: boolean,
+  isDismissable?: boolean
 }
 
 /**
@@ -47,7 +48,18 @@ let arrowPlacement = {
 };
 
 function Popover(props: PopoverProps, ref: DOMRef<HTMLDivElement>) {
-  let {children, placement, arrowProps, onClose, shouldCloseOnBlur, hideArrow, isKeyboardDismissDisabled, isNonModal, ...otherProps} = props;
+  let {
+    children,
+    placement,
+    arrowProps,
+    onClose,
+    shouldCloseOnBlur,
+    hideArrow,
+    isKeyboardDismissDisabled,
+    isNonModal,
+    isDismissable = true,
+    ...otherProps
+  } = props;
   let domRef = useDOMRef(ref);
   let {styleProps} = useStyleProps(props);
 
@@ -62,7 +74,8 @@ function Popover(props: PopoverProps, ref: DOMRef<HTMLDivElement>) {
         shouldCloseOnBlur={shouldCloseOnBlur}
         isKeyboardDismissDisabled={isKeyboardDismissDisabled}
         hideArrow={hideArrow}
-        isNonModal={isNonModal}>
+        isNonModal={isNonModal}
+        isDismissable={isDismissable}>
         {children}
       </PopoverWrapper>
     </Overlay>
@@ -70,9 +83,22 @@ function Popover(props: PopoverProps, ref: DOMRef<HTMLDivElement>) {
 }
 
 const PopoverWrapper = forwardRef((props: PopoverWrapperProps, ref: RefObject<HTMLDivElement>) => {
-  // eslint-disable-next-line @typescript-eslint/no-unused-vars
-  let {children, placement = 'bottom', arrowProps, isOpen, hideArrow, shouldCloseOnBlur, isKeyboardDismissDisabled, isNonModal, ...otherProps} = props;
-  let {overlayProps} = useOverlay({...props, isDismissable: true}, ref);
+  let {
+    children,
+    placement = 'bottom',
+    arrowProps,
+    isOpen,
+    hideArrow,
+    // eslint-disable-next-line @typescript-eslint/no-unused-vars
+    shouldCloseOnBlur,
+    // eslint-disable-next-line @typescript-eslint/no-unused-vars
+    isKeyboardDismissDisabled,
+    isNonModal,
+    // eslint-disable-next-line @typescript-eslint/no-unused-vars
+    isDismissable,
+    ...otherProps
+  } = props;
+  let {overlayProps} = useOverlay({...props, isDismissable: isDismissable && isOpen}, ref);
   let {modalProps} = useModal({
     isDisabled: isNonModal
   });
diff --git a/packages/@react-types/overlays/src/index.d.ts b/packages/@react-types/overlays/src/index.d.ts
index e149bf73561..abdb5a79467 100644
--- a/packages/@react-types/overlays/src/index.d.ts
+++ b/packages/@react-types/overlays/src/index.d.ts
@@ -90,7 +90,8 @@ export interface PopoverProps extends StyleProps, OverlayProps {
   isOpen?: boolean,
   onClose?: () => void,
   shouldCloseOnBlur?: boolean,
-  isNonModal?: boolean
+  isNonModal?: boolean,
+  isDismissable?: boolean
 }
 
 export interface TrayProps extends StyleProps, OverlayProps {