diff --git a/packages/components/CHANGELOG.md b/packages/components/CHANGELOG.md
index 5e0e1d9563d219..9bdfec755a5ca2 100644
--- a/packages/components/CHANGELOG.md
+++ b/packages/components/CHANGELOG.md
@@ -13,6 +13,7 @@
 -   `Popover`: enable auto-updating every animation frame ([#43617](https://github.com/WordPress/gutenberg/pull/43617)).
 -   `Popover`: improve the component's performance and reactivity to prop changes by reworking its internals ([#43335](https://github.com/WordPress/gutenberg/pull/43335)).
 -   `NavigatorScreen`: updated to satisfy `react/exhaustive-deps` eslint rule ([#43876](https://github.com/WordPress/gutenberg/pull/43876))
+-   `Popover`: fix positioning when reference and floating elements are both within an iframe ([#43971](https://github.com/WordPress/gutenberg/pull/43971))
 
 ### Enhancements
 
diff --git a/packages/components/src/popover/index.tsx b/packages/components/src/popover/index.tsx
index a566e259a84f52..905943fc7cba27 100644
--- a/packages/components/src/popover/index.tsx
+++ b/packages/components/src/popover/index.tsx
@@ -416,10 +416,12 @@ const UnforwardedPopover = (
 	// document scrolls. Also update the frame offset if the view resizes.
 	useLayoutEffect( () => {
 		if (
-			// reference and floating are in the same document
+			// Reference and root documents are the same.
 			referenceOwnerDocument === document ||
-			// the reference's document has a view (i.e. window)
-			// and a frame element (ie. it's an iframe)
+			// Reference and floating are in the same document.
+			referenceOwnerDocument === refs?.floating?.current?.ownerDocument ||
+			// The reference's document has no view (i.e. window)
+			// or frame element (ie. it's not an iframe).
 			! referenceOwnerDocument?.defaultView?.frameElement
 		) {
 			frameOffsetRef.current = undefined;