diff --git a/resources/skins.vector.es6/main.js b/resources/skins.vector.es6/main.js
index f3ac530c9..31d65dc5b 100644
--- a/resources/skins.vector.es6/main.js
+++ b/resources/skins.vector.es6/main.js
@@ -278,7 +278,10 @@ const main = () => {
 		onToggleClick: ( id ) => {
 			tableOfContents.toggleExpandSection( id );
 		},
-		onTogglePinned: updateTocLocation
+		onTogglePinned: () => {
+			updateTocLocation();
+			pinnableElement.setFocusAfterToggle( TOC_ID );
+		}
 	} );
 	const headingSelector = [
 		'h1', 'h2', 'h3', 'h4', 'h5', 'h6'
diff --git a/resources/skins.vector.es6/pinnableElement.js b/resources/skins.vector.es6/pinnableElement.js
index a8b786b3e..69d004e55 100644
--- a/resources/skins.vector.es6/pinnableElement.js
+++ b/resources/skins.vector.es6/pinnableElement.js
@@ -97,14 +97,39 @@ function pinnableElementClickHandler( header ) {
 	} = header.dataset;
 
 	togglePinnableClasses( header );
+	setSavedPinnableState( header );
 
 	// Optional functionality of moving the pinnable element in the DOM
 	// to different containers based on it's pinned status
 	if ( pinnableElementId && pinnedContainerId && unpinnedContainerId ) {
 		const newContainerId = isPinned( header ) ? pinnedContainerId : unpinnedContainerId;
 		movePinnableElement( pinnableElementId, newContainerId );
+		setFocusAfterToggle( pinnableElementId );
+	}
+}
+
+/**
+ * Sets focus on the correct toggle button depending on the pinned state.
+ * Also opens the dropdown containing the unpinned element.
+ *
+ * @param {string} pinnableElementId
+ */
+function setFocusAfterToggle( pinnableElementId ) {
+	let focusElement;
+	const pinnableElement = document.getElementById( pinnableElementId );
+	const header = /** @type {HTMLElement|null} */ ( pinnableElement && pinnableElement.querySelector( '.vector-pinnable-header' ) );
+	if ( !pinnableElement || !header ) {
+		return;
+	}
+	if ( isPinned( header ) ) {
+		focusElement = /** @type {HTMLElement|null} */ ( pinnableElement.querySelector( '.vector-pinnable-header-unpin-button' ) );
+	} else {
+		const dropdown = pinnableElement.closest( '.vector-dropdown' );
+		focusElement = /** @type {HTMLInputElement|null} */ ( dropdown && dropdown.querySelector( '.vector-menu-checkbox' ) );
+	}
+	if ( focusElement ) {
+		focusElement.focus();
 	}
-	setSavedPinnableState( header );
 }
 
 /**
@@ -177,6 +202,7 @@ function initPinnableElement() {
 module.exports = {
 	initPinnableElement,
 	movePinnableElement,
+	setFocusAfterToggle,
 	isPinned,
 	PINNED_HEADER_CLASS,
 	UNPINNED_HEADER_CLASS
diff --git a/tests/jest/__snapshots__/pinnableElement.test.js.snap b/tests/jest/__snapshots__/pinnableElement.test.js.snap
index bb5391172..cb4c28d9c 100644
--- a/tests/jest/__snapshots__/pinnableElement.test.js.snap
+++ b/tests/jest/__snapshots__/pinnableElement.test.js.snap
@@ -5,13 +5,21 @@ exports[`Pinnable header renders 1`] = `
 		<div id=\\"pinned-container\\">
 			
 		</div>
-		<div id=\\"unpinned-container\\">
-			<div id=\\"pinnable-element\\"> <div class=\\"vector-pinnable-header simple-pinnable-header vector-pinnable-header-unpinned\\" data-name=\\"simple\\" data-pinnable-element-id=\\"pinnable-element\\">
+		<div class=\\"vector-dropdown\\">
+			<input type=\\"checkbox\\" id=\\"checkbox\\" class=\\"vector-menu-checkbox\\">
+			<label for=\\"checkbox\\" class=\\"vector-menu-heading \\">
+				<span class=\\"vector-menu-heading-label\\">Dropdown</span>
+			</label>
+			<div class=\\"vector-menu-content\\">
+				<div id=\\"unpinned-container\\">
+				<div id=\\"pinnable-element\\"> <div class=\\"vector-pinnable-header simple-pinnable-header vector-pinnable-header-unpinned\\" data-name=\\"simple\\" data-pinnable-element-id=\\"pinnable-element\\">
 	<div class=\\"vector-pinnable-header-label\\">simple pinnable element</div>
 	<button class=\\"vector-pinnable-header-toggle-button vector-pinnable-header-pin-button\\" data-event-name=\\"pinnable-header.simple.pin\\">pin</button>
 	<button class=\\"vector-pinnable-header-toggle-button vector-pinnable-header-unpin-button\\" data-event-name=\\"pinnable-header.simple.unpin\\">unpin</button>
 </div>
  </div>
+				</div>
+			</div>
 		</div>
 	"
 `;
diff --git a/tests/jest/pinnableElement.test.js b/tests/jest/pinnableElement.test.js
index 3b0549f07..ce17a055b 100644
--- a/tests/jest/pinnableElement.test.js
+++ b/tests/jest/pinnableElement.test.js
@@ -54,8 +54,16 @@ const initializeHTML = ( headerData ) => {
 		<div id="pinned-container">
 			${ headerData[ 'is-pinned' ] ? pinnableElementHTML : '' }
 		</div>
-		<div id="unpinned-container">
-			${ !headerData[ 'is-pinned' ] ? pinnableElementHTML : '' }
+		<div class="vector-dropdown">
+			<input type="checkbox" id="checkbox" class="vector-menu-checkbox">
+			<label for="checkbox" class="vector-menu-heading ">
+				<span class="vector-menu-heading-label">Dropdown</span>
+			</label>
+			<div class="vector-menu-content">
+				<div id="unpinned-container">
+				${ !headerData[ 'is-pinned' ] ? pinnableElementHTML : '' }
+				</div>
+			</div>
 		</div>
 	`;
 
@@ -173,4 +181,17 @@ describe( 'Pinnable header', () => {
 
 		expect( pinnableElement.isPinned( header ) ).toBe( false );
 	} );
+
+	test( 'setFocusAfterToggle() sets focus on appropriate element after pinnableElement is toggled', () => {
+		initializeHTML( movableData );
+		pinnableElement.initPinnableElement();
+		const dropdownCheckbox = /** @type {HTMLElement} */ ( document.getElementById( 'checkbox' ) );
+		const pinButton = /** @type {HTMLElement} */ ( document.querySelector( '.vector-pinnable-header-pin-button' ) );
+		const unpinButton = /** @type {HTMLElement} */ ( document.querySelector( '.vector-pinnable-header-unpin-button' ) );
+
+		pinButton.click();
+		expect( document.activeElement ).toBe( unpinButton );
+		unpinButton.click();
+		expect( document.activeElement ).toBe( dropdownCheckbox );
+	} );
 } );