diff --git a/projects/igniteui-angular/directives/src/directives/for-of/for_of.directive.spec.ts b/projects/igniteui-angular/directives/src/directives/for-of/for_of.directive.spec.ts
index 81d87eab2fc..d6c252db2cb 100644
--- a/projects/igniteui-angular/directives/src/directives/for-of/for_of.directive.spec.ts
+++ b/projects/igniteui-angular/directives/src/directives/for-of/for_of.directive.spec.ts
@@ -379,6 +379,75 @@ describe('IgxForOf directive -', () => {
             node.remove();
         });
 
+        it('should resolve the observed node from a comment-rooted view', () => {
+            const virtualContainer = fix.componentInstance.parentVirtDir;
+            const anchor = document.createComment('container');
+            const element = document.createElement('div');
+            fix.nativeElement.appendChild(anchor);
+            fix.nativeElement.appendChild(element);
+
+            // A control flow root leaves only comment anchors among the root
+            // nodes; the rendered element follows the first of them.
+            expect(virtualContainer.testGetViewObservedNode({ rootNodes: [anchor] })).toBe(element);
+
+            anchor.remove();
+            element.remove();
+        });
+
+        it('should resolve no observed node when the view holds no element', () => {
+            const virtualContainer = fix.componentInstance.parentVirtDir;
+            const orphan = document.createComment('container');
+            fix.nativeElement.appendChild(orphan);
+
+            // Nothing follows the anchor - the view was torn down before its
+            // content rendered.
+            expect(virtualContainer.testGetViewObservedNode({ rootNodes: [orphan] })).toBeNull();
+            expect(virtualContainer.testGetViewObservedNode({ rootNodes: [] })).toBeNull();
+            expect(virtualContainer.testGetViewObservedNode(null)).toBeNull();
+
+            orphan.remove();
+        });
+
+        it('should not unobserve a view that resolves to no element', () => {
+            const virtualContainer = fix.componentInstance.parentVirtDir;
+            const observer = jasmine.createSpyObj<ResizeObserver>('ResizeObserver', [
+                'observe',
+                'unobserve',
+                'disconnect'
+            ]);
+            virtualContainer.testSetViewObserver(observer);
+
+            // A comment anchor with no element after it - ResizeObserver.unobserve()
+            // throws on anything that is not an Element.
+            const orphan = document.createComment('container');
+            virtualContainer.testSetEmbeddedViews([{ rootNodes: [orphan], destroy: () => { } }]);
+
+            expect(() => virtualContainer.testRemoveLastElem()).not.toThrow();
+            expect(observer.unobserve).not.toHaveBeenCalled();
+        });
+
+        it('should unobserve the element that follows a comment-rooted view', () => {
+            const virtualContainer = fix.componentInstance.parentVirtDir;
+            const observer = jasmine.createSpyObj<ResizeObserver>('ResizeObserver', [
+                'observe',
+                'unobserve',
+                'disconnect'
+            ]);
+            virtualContainer.testSetViewObserver(observer);
+
+            const anchor = document.createComment('container');
+            const element = document.createElement('div');
+            fix.nativeElement.appendChild(anchor);
+            fix.nativeElement.appendChild(element);
+            virtualContainer.testSetEmbeddedViews([{ rootNodes: [anchor], destroy: () => { } }]);
+
+            virtualContainer.testRemoveLastElem();
+            expect(observer.unobserve).toHaveBeenCalledWith(element);
+
+            anchor.remove();
+            element.remove();
+        });
+
         it('should preserve valid border sizes when another side cannot be parsed', () => {
             const virtualContainer = fix.componentInstance.parentVirtDir;
             const node = document.createElement('div');
@@ -1426,6 +1495,22 @@ export class TestIgxForOfDirective<T> extends IgxForOfDirective<T> {
     public testGetBorder(node: Element, dimension: string): number {
         return super.getBorder(node, dimension);
     }
+
+    public testGetViewObservedNode(view: any): Element | null {
+        return super.getViewObservedNode(view);
+    }
+
+    public testRemoveLastElem(): void {
+        super.removeLastElem();
+    }
+
+    public testSetEmbeddedViews(views: any[]): void {
+        this._embeddedViews = views;
+    }
+
+    public testSetViewObserver(observer: ResizeObserver): void {
+        this.viewObserver = observer;
+    }
 }
 
 /** Empty virtualized component */
diff --git a/projects/igniteui-angular/directives/src/directives/for-of/for_of.directive.ts b/projects/igniteui-angular/directives/src/directives/for-of/for_of.directive.ts
index b1ce3e59401..9bc1e8cfb19 100644
--- a/projects/igniteui-angular/directives/src/directives/for-of/for_of.directive.ts
+++ b/projects/igniteui-angular/directives/src/directives/for-of/for_of.directive.ts
@@ -523,7 +523,28 @@ export class IgxForOfDirective<T, U extends T[] = T[]> extends IgxForOfToken<T,U
         }
     }
 
-    protected subscribeToViewObserver(target: Element) {
+    /**
+     * @hidden
+     * Resolves the element a view is tracked by.
+     *
+     * The view's root nodes are not always elements: when the template's root is
+     * a control flow block they are comment anchors, and the rendered element
+     * follows the first of them. Both lookups can come up empty - the view may
+     * hold no element at all, or be torn down before its content is rendered -
+     * in which case there is nothing to observe and null is returned.
+     */
+    protected getViewObservedNode(view: EmbeddedViewRef<any> | null | undefined): Element | null {
+        const rootNodes = view?.rootNodes ?? [];
+        const elementNode = rootNodes.find(node=> node?.nodeType === Node.ELEMENT_NODE);
+        const candidate = elementNode ?? rootNodes[0]?.nextElementSibling;
+        return candidate?.nodeType === Node.ELEMENT_NODE ? candidate : null;
+    }
+
+    protected subscribeToViewObserver(target: Element | null) {
+        if (!target) {
+            return;
+        }
+
         if (this.igxForScrollOrientation === 'vertical' && this.viewObserver) {
             this._zone.runOutsideAngular(() => {
                 if (this.platformUtil.isBrowser) {
@@ -1456,7 +1477,16 @@ export class IgxForOfDirective<T, U extends T[] = T[]> extends IgxForOfToken<T,U
     protected removeLastElem() {
         const oldElem = this._embeddedViews.pop();
         this.beforeViewDestroyed.emit(oldElem);
-        this.viewObserver?.unobserve(oldElem.rootNodes.find(node => node.nodeType === Node.ELEMENT_NODE) || oldElem.rootNodes[0].nextElementSibling);
+        // The observed node is not necessarily a root node of the view: when the
+        // template's root is a control flow block the root nodes are comment
+        // anchors, and the rendered element follows the first of them. Either
+        // lookup can come up empty - the view may hold no element at all, or be
+        // torn down before its content is rendered - and ResizeObserver throws
+        // on anything that is not an Element.
+        const observedNode = this.getViewObservedNode(oldElem);
+        if (observedNode) {
+            this.viewObserver?.unobserve(observedNode);
+        }
         // also detach from ViewContainerRef to make absolutely sure this is removed from the view container.
         this.dc.instance._vcr.detach(this.dc.instance._vcr.length - 1);
         oldElem.destroy();
@@ -1930,7 +1960,7 @@ export class IgxGridForOfDirective<T, U extends T[] = T[]> extends IgxForOfDirec
         );
 
         this._embeddedViews.push(embeddedView);
-        this.subscribeToViewObserver(embeddedView.rootNodes.find(node => node.nodeType === Node.ELEMENT_NODE) || embeddedView.rootNodes[0].nextElementSibling);
+        this.subscribeToViewObserver(this.getViewObservedNode(embeddedView));
         this.state.chunkSize++;
     }