diff --git a/packages/components/src/higher-order/with-constrained-tabbing/index.js b/packages/components/src/higher-order/with-constrained-tabbing/index.js
index 8d1574e0a20197..75745cc9d02429 100644
--- a/packages/components/src/higher-order/with-constrained-tabbing/index.js
+++ b/packages/components/src/higher-order/with-constrained-tabbing/index.js
@@ -33,6 +33,13 @@ const withConstrainedTabbing = createHigherOrderComponent(
 			} else if ( ! event.shiftKey && event.target === lastTabbable ) {
 				event.preventDefault();
 				firstTabbable.focus();
+			/*
+			 * When pressing Tab and none of the tabbables has focus, the keydown
+			 * event happens on the wrapper div: move focus on the first tabbable.
+			 */
+			} else if ( ! tabbables.includes( event.target ) ) {
+				event.preventDefault();
+				firstTabbable.focus();
 			}
 		}
 
@@ -44,6 +51,7 @@ const withConstrainedTabbing = createHigherOrderComponent(
 				<div
 					onKeyDown={ this.handleTabBehaviour }
 					ref={ this.focusContainRef }
+					tabIndex="-1"
 				>
 					<WrappedComponent { ...this.props } />
 				</div>
diff --git a/test/e2e/specs/a11y.test.js b/test/e2e/specs/a11y.test.js
index 4a15f7ccf8668e..704ae68bba49e4 100644
--- a/test/e2e/specs/a11y.test.js
+++ b/test/e2e/specs/a11y.test.js
@@ -1,10 +1,20 @@
 /**
  * Internal dependencies
  */
-import { newPost, pressWithModifier } from '../support/utils';
+import {
+	ACCESS_MODIFIER_KEYS,
+	newPost,
+	pressWithModifier,
+} from '../support/utils';
+
+function isCloseButtonFocused() {
+	return page.$eval( ':focus', ( focusedElement ) => {
+		return focusedElement.getAttribute( 'aria-label' ) === 'Close dialog';
+	} );
+}
 
 describe( 'a11y', () => {
-	beforeAll( async () => {
+	beforeEach( async () => {
 		await newPost();
 	} );
 
@@ -19,4 +29,43 @@ describe( 'a11y', () => {
 
 		expect( isFocusedToggle ).toBe( true );
 	} );
+
+	it( 'constrains focus to a modal when tabbing', async () => {
+		// Open help modal
+		await pressWithModifier( ACCESS_MODIFIER_KEYS, 'h' );
+
+		// Test that the Close button of the modal is focused when the
+		// latter is opened.
+		expect( await isCloseButtonFocused() ).toBe( true );
+
+		await page.keyboard.press( 'Tab' );
+
+		// Test that the Close button of the modal is focused when the
+		// latter is opened.
+		expect( await isCloseButtonFocused() ).toBe( true );
+	} );
+
+	it( 'returns focus to the first tabbable in a modal after blurring a tabbable', async () => {
+		await pressWithModifier( ACCESS_MODIFIER_KEYS, 'h' );
+
+		// Click to move focus to an element after the last tabbable within the
+		// modal.
+		await page.click( '.components-modal__content' );
+
+		await page.keyboard.press( 'Tab' );
+
+		expect( await isCloseButtonFocused() ).toBe( true );
+	} );
+
+	it( 'returns focus to the last tabbable in a modal after blurring a tabbable and tabbing in reverse direction', async () => {
+		await pressWithModifier( ACCESS_MODIFIER_KEYS, 'h' );
+
+		// Click to move focus to an element before the first tabbable within
+		// the modal.
+		await page.click( '.components-modal__header-heading' );
+
+		await pressWithModifier( 'Shift', 'Tab' );
+
+		expect( await isCloseButtonFocused() ).toBe( true );
+	} );
 } );