diff --git a/packages/block-editor/src/components/block-list/block-popover.js b/packages/block-editor/src/components/block-list/block-popover.js
index cb563c3319f21..8f04a3571aa73 100644
--- a/packages/block-editor/src/components/block-list/block-popover.js
+++ b/packages/block-editor/src/components/block-list/block-popover.js
@@ -128,11 +128,15 @@ function BlockPopover( {
 			className="block-editor-block-list__block-popover"
 			__unstableSticky={ showEmptyBlockSideInserter ? false : popoverIsSticky }
 			__unstableSlotName="block-toolbar"
+			__unstableBoundaryParent
 			// Allow subpixel positioning for the block movement animation.
 			__unstableAllowVerticalSubpixelPosition={ moverDirection !== 'horizontal' && node }
 			__unstableAllowHorizontalSubpixelPosition={ moverDirection === 'horizontal' && node }
 			onBlur={ () => setIsToolbarForced( false ) }
 			shouldAnchorIncludePadding
+			// Popover calculates the width once. Trigger a reset by remounting
+			// the component.
+			key={ shouldShowContextualToolbar }
 		>
 			{ ( shouldShowContextualToolbar || isToolbarForced ) && (
 				<div
diff --git a/packages/components/src/popover/index.js b/packages/components/src/popover/index.js
index ca1b953c27ee1..3b456b7ac11f0 100644
--- a/packages/components/src/popover/index.js
+++ b/packages/components/src/popover/index.js
@@ -228,6 +228,7 @@ const Popover = ( {
 	__unstableSlotName = SLOT_NAME,
 	__unstableAllowVerticalSubpixelPosition,
 	__unstableAllowHorizontalSubpixelPosition,
+	__unstableBoundaryParent,
 	/* eslint-enable no-unused-vars */
 	...contentProps
 } ) => {
@@ -273,6 +274,12 @@ const Popover = ( {
 				contentRect.current = contentRef.current.getBoundingClientRect();
 			}
 
+			let boundaryElement;
+
+			if ( __unstableBoundaryParent ) {
+				boundaryElement = containerRef.current.closest( '.popover-slot' ).parentNode;
+			}
+
 			const {
 				popoverTop,
 				popoverLeft,
@@ -280,7 +287,14 @@ const Popover = ( {
 				yAxis,
 				contentHeight,
 				contentWidth,
-			} = computePopoverPosition( anchor, contentRect.current, position, __unstableSticky, anchorRef );
+			} = computePopoverPosition(
+				anchor,
+				contentRect.current,
+				position,
+				__unstableSticky,
+				anchorRef,
+				boundaryElement
+			);
 
 			if ( typeof popoverTop === 'number' && typeof popoverLeft === 'number' ) {
 				if ( subpixels && __unstableAllowVerticalSubpixelPosition ) {
@@ -374,6 +388,7 @@ const Popover = ( {
 		__unstableSticky,
 		__unstableAllowVerticalSubpixelPosition,
 		__unstableAllowHorizontalSubpixelPosition,
+		__unstableBoundaryParent,
 	] );
 
 	useFocusContentOnMount( focusOnMount, contentRef );
@@ -511,6 +526,6 @@ const Popover = ( {
 const PopoverContainer = Popover;
 
 PopoverContainer.Slot = ( { name = SLOT_NAME } ) =>
-	<Slot bubblesVirtually name={ name } />;
+	<Slot bubblesVirtually name={ name } className="popover-slot" />;
 
 export default PopoverContainer;
diff --git a/packages/components/src/popover/utils.js b/packages/components/src/popover/utils.js
index 971ec4919d1c9..05ebfc7896be7 100644
--- a/packages/components/src/popover/utils.js
+++ b/packages/components/src/popover/utils.js
@@ -19,10 +19,11 @@ const HEIGHT_OFFSET = 10; // used by the arrow and a bit of empty space
  *                              scroll container edge when part of the anchor
  *                              leaves view.
  * @param {string}  chosenYAxis yAxis to be used.
+ * @param {Element} boundaryElement
  *
  * @return {Object} Popover xAxis position and constraints.
  */
-export function computePopoverXAxisPosition( anchorRect, contentSize, xAxis, corner, sticky, chosenYAxis ) {
+export function computePopoverXAxisPosition( anchorRect, contentSize, xAxis, corner, sticky, chosenYAxis, boundaryElement ) {
 	const { width } = contentSize;
 	const isRTL = document.documentElement.dir === 'rtl';
 
@@ -101,6 +102,11 @@ export function computePopoverXAxisPosition( anchorRect, contentSize, xAxis, cor
 		popoverLeft = rightAlignment.popoverLeft;
 	}
 
+	if ( boundaryElement ) {
+		const boundaryRect = boundaryElement.getBoundingClientRect();
+		popoverLeft = Math.min( popoverLeft, boundaryRect.right - width );
+	}
+
 	return {
 		xAxis: chosenXAxis,
 		popoverLeft,
@@ -222,14 +228,22 @@ export function computePopoverYAxisPosition( anchorRect, contentSize, yAxis, cor
  *                              scroll container edge when part of the anchor
  *                              leaves view.
  * @param {Element} anchorRef   The anchor element.
+ * @param {Element} boundaryElement
  *
  * @return {Object} Popover position and constraints.
  */
-export function computePopoverPosition( anchorRect, contentSize, position = 'top', sticky, anchorRef ) {
+export function computePopoverPosition(
+	anchorRect,
+	contentSize,
+	position = 'top',
+	sticky,
+	anchorRef,
+	boundaryElement
+) {
 	const [ yAxis, xAxis = 'center', corner ] = position.split( ' ' );
 
 	const yAxisPosition = computePopoverYAxisPosition( anchorRect, contentSize, yAxis, corner, sticky, anchorRef );
-	const xAxisPosition = computePopoverXAxisPosition( anchorRect, contentSize, xAxis, corner, sticky, yAxisPosition.yAxis );
+	const xAxisPosition = computePopoverXAxisPosition( anchorRect, contentSize, xAxis, corner, sticky, yAxisPosition.yAxis, boundaryElement );
 
 	return {
 		...xAxisPosition,