diff --git a/components/popover/index.js b/components/popover/index.js
index f10e52f2d60ab..df975fd536975 100644
--- a/components/popover/index.js
+++ b/components/popover/index.js
@@ -2,7 +2,7 @@
  * External dependencies
  */
 import classnames from 'classnames';
-import { isEqual, noop } from 'lodash';
+import { defer, isEqual, noop } from 'lodash';
 
 /**
  * WordPress dependencies
@@ -19,6 +19,19 @@ import PopoverDetectOutside from './detect-outside';
 import IconButton from '../icon-button';
 import { Slot, Fill } from '../slot-fill';
 
+/**
+ * Value representing whether a key is currently pressed. Bound to the document
+ * for use in determining whether the Popover component has mounted in response
+ * to a keyboard event. Popover's focusOnMount behavior is specific to keyboard
+ * interaction. Must be bound at the top-level and its unsetting deferred since
+ * the component will have already mounted by the time keyup occurs.
+ *
+ * @type {boolean}
+ */
+let isKeyDown = false;
+document.addEventListener( 'keydown', () => isKeyDown = true );
+document.addEventListener( 'keyup', defer.bind( null, () => isKeyDown = false ) );
+
 const FocusManaged = withFocusReturn( ( { children } ) => children );
 
 const { ESCAPE } = keycodes;
@@ -94,7 +107,7 @@ class Popover extends Component {
 
 	focus() {
 		const { focusOnMount = true } = this.props;
-		if ( ! focusOnMount ) {
+		if ( ! focusOnMount || ! isKeyDown ) {
 			return;
 		}
 
diff --git a/components/popover/test/index.js b/components/popover/test/index.js
index 8fa4b179a2ed7..f6bb7dbe7eccc 100644
--- a/components/popover/test/index.js
+++ b/components/popover/test/index.js
@@ -25,6 +25,14 @@ describe( 'Popover', () => {
 
 		afterEach( () => {
 			jest.restoreAllMocks();
+
+			// Resetting keyboard state is deferred, so ensure that timers are
+			// consumed to avoid leaking into other tests.
+			jest.runAllTimers();
+
+			if ( document.activeElement ) {
+				document.activeElement.blur();
+			}
 		} );
 
 		it( 'should add window events', () => {
@@ -59,7 +67,12 @@ describe( 'Popover', () => {
 			expect( Popover.prototype.setForcedPositions ).not.toHaveBeenCalled();
 		} );
 
-		it( 'should focus when opening', () => {
+		it( 'should focus when opening in response to keyboard event', () => {
+			// As in the real world, these occur in sequence before the popover
+			// has been mounted. Keyup's resetting is deferred.
+			document.dispatchEvent( new window.KeyboardEvent( 'keydown' ) );
+			document.dispatchEvent( new window.KeyboardEvent( 'keyup' ) );
+
 			// An ideal test here would mount with an input child and focus the
 			// child, but in context of JSDOM the inputs are not visible and
 			// are therefore skipped as tabbable, defaulting to popover.
@@ -70,6 +83,12 @@ describe( 'Popover', () => {
 			expect( document.activeElement ).toBe( content );
 		} );
 
+		it( 'should not focus when opening in response to pointer event', () => {
+			wrapper = mount( <Popover /> );
+
+			expect( document.activeElement ).toBe( document.body );
+		} );
+
 		it( 'should allow focus-on-open behavior to be disabled', () => {
 			const activeElement = document.activeElement;