diff --git a/UNRELEASED.md b/UNRELEASED.md
index ea91b1bdc80..14b2a598a6f 100644
--- a/UNRELEASED.md
+++ b/UNRELEASED.md
@@ -15,6 +15,7 @@ Use [the changelog guidelines](https://git.io/polaris-changelog-guidelines) to f
 - Fixed tabs that don't wrap correctly on small screens in pre-iOS 13 Safari ([#2232](https://github.com/Shopify/polaris-react/pull/2232))
 - Fixed `BulkActions` checkbox losing on selection focus ([#2138](https://github.com/Shopify/polaris-react/pull/2138))
 - Moved rendering of the portal component’s node within the node created by the theme provider component to enable theming through CSS Custom Properties ([#2224](https://github.com/Shopify/polaris-react/pull/2224))
+- Fixed bug which caused the `Popover` overlay to remain in the DOM if it was updated during exiting ([#2246](https://github.com/Shopify/polaris-react/pull/2246))
 
 ### Documentation
 
diff --git a/src/components/Popover/components/PopoverOverlay/PopoverOverlay.tsx b/src/components/Popover/components/PopoverOverlay/PopoverOverlay.tsx
index 2ff8b59f766..b88e2d10d98 100644
--- a/src/components/Popover/components/PopoverOverlay/PopoverOverlay.tsx
+++ b/src/components/Popover/components/PopoverOverlay/PopoverOverlay.tsx
@@ -85,11 +85,10 @@ export class PopoverOverlay extends React.PureComponent<
   }
 
   componentDidUpdate(oldProps: PopoverOverlayProps) {
-    this.clearTransitionTimeout();
-
     if (this.props.active && !oldProps.active) {
       this.focusContent();
       this.changeTransitionStatus(TransitionStatus.Entering, () => {
+        this.clearTransitionTimeout();
         this.enteringTimer = window.setTimeout(() => {
           this.setState({transitionStatus: TransitionStatus.Entered});
         }, durationBase);
@@ -98,6 +97,7 @@ export class PopoverOverlay extends React.PureComponent<
 
     if (!this.props.active && oldProps.active) {
       this.changeTransitionStatus(TransitionStatus.Exiting, () => {
+        this.clearTransitionTimeout();
         this.exitingTimer = window.setTimeout(() => {
           this.setState({transitionStatus: TransitionStatus.Exited});
         }, durationBase);
diff --git a/src/components/Popover/components/PopoverOverlay/tests/PopoverOverlay.test.tsx b/src/components/Popover/components/PopoverOverlay/tests/PopoverOverlay.test.tsx
index 75f859f3f41..95c173ca6e7 100644
--- a/src/components/Popover/components/PopoverOverlay/tests/PopoverOverlay.test.tsx
+++ b/src/components/Popover/components/PopoverOverlay/tests/PopoverOverlay.test.tsx
@@ -1,4 +1,5 @@
 import React from 'react';
+import {ReactWrapper} from 'enzyme';
 import {mountWithAppProvider} from 'test-utilities/legacy';
 import {TextContainer} from 'components';
 import {Key} from '../../../../../types';
@@ -174,6 +175,43 @@ describe('<PopoverOverlay />', () => {
       /PopoverOverlay-entering/,
     );
   });
+
+  it('does not render after exiting when the component is updated during exit', () => {
+    jest.useFakeTimers();
+
+    const popoverOverlay = mountWithAppProvider(
+      <PopoverOverlay
+        active
+        id="PopoverOverlay-1"
+        activator={activator}
+        onClose={noop}
+      >
+        {children}
+      </PopoverOverlay>,
+    );
+
+    // Start exiting
+    close(popoverOverlay);
+
+    // Update before exiting is complete
+    triggerSomeUpdate(popoverOverlay);
+
+    // Run any timers and a final update for changed state
+    jest.runOnlyPendingTimers();
+    popoverOverlay.update();
+
+    expect(popoverOverlay.find(PositionedOverlay)).toHaveLength(0);
+  });
 });
 
 function noop() {}
+
+function close(wrapper: ReactWrapper) {
+  wrapper.setProps({active: false});
+  wrapper.update();
+}
+
+function triggerSomeUpdate(wrapper: ReactWrapper) {
+  wrapper.setProps({fullWidth: true});
+  wrapper.update();
+}