diff --git a/packages/block-editor/src/components/block-popover/use-popover-scroll.js b/packages/block-editor/src/components/block-popover/use-popover-scroll.js
index 5dfa74005a4081..2d3158e57d0ba7 100644
--- a/packages/block-editor/src/components/block-popover/use-popover-scroll.js
+++ b/packages/block-editor/src/components/block-popover/use-popover-scroll.js
@@ -17,14 +17,22 @@ function usePopoverScroll( contentRef ) {
 	const effect = useRefEffect(
 		( node ) => {
 			function onWheel( event ) {
-				const { deltaX, deltaY } = event;
+				const { deltaX, deltaY, target } = event;
 				const contentEl = contentRef.current;
 				let scrollContainer = scrollContainerCache.get( contentEl );
 				if ( ! scrollContainer ) {
 					scrollContainer = getScrollContainer( contentEl );
 					scrollContainerCache.set( contentEl, scrollContainer );
 				}
-				scrollContainer.scrollBy( deltaX, deltaY );
+				// Finds a scrollable ancestor of the event’s target. It's not cached because the
+				// it may not remain scrollable due to popover position changes. The cache is also
+				// less likely to be utilized because the target may be different every event.
+				const eventScrollContainer = getScrollContainer( target );
+				// Scrolls “through” the popover only if another contained scrollable area isn’t
+				// in front of it. This is to avoid scrolling both containers simultaneously.
+				if ( ! node.contains( eventScrollContainer ) ) {
+					scrollContainer.scrollBy( deltaX, deltaY );
+				}
 			}
 			// Tell the browser that we do not call event.preventDefault
 			// See https://developer.mozilla.org/en-US/docs/Web/API/EventTarget/addEventListener#improving_scrolling_performance_with_passive_listeners