diff --git a/packages/overlay/src/vaadin-overlay-position-mixin.js b/packages/overlay/src/vaadin-overlay-position-mixin.js
index 988d0cf79d..9bec60ecfe 100644
--- a/packages/overlay/src/vaadin-overlay-position-mixin.js
+++ b/packages/overlay/src/vaadin-overlay-position-mixin.js
@@ -146,9 +146,12 @@ export const PositionMixin = (superClass) =>
 
     /** @private */
     __addUpdatePositionEventListeners() {
-      window.addEventListener('resize', this._updatePosition);
+      window.visualViewport.addEventListener('resize', this._updatePosition);
+      window.visualViewport.addEventListener('scroll', this.__onScroll, true);
 
-      this.__positionTargetAncestorRootNodes = getAncestorRootNodes(this.positionTarget);
+      this.__positionTargetAncestorRootNodes = getAncestorRootNodes(this.positionTarget).filter(
+        (node) => node !== document,
+      );
       this.__positionTargetAncestorRootNodes.forEach((node) => {
         node.addEventListener('scroll', this.__onScroll, true);
       });
@@ -156,7 +159,8 @@ export const PositionMixin = (superClass) =>
 
     /** @private */
     __removeUpdatePositionEventListeners() {
-      window.removeEventListener('resize', this._updatePosition);
+      window.visualViewport.removeEventListener('resize', this._updatePosition);
+      window.visualViewport.removeEventListener('scroll', this.__onScroll, true);
 
       if (this.__positionTargetAncestorRootNodes) {
         this.__positionTargetAncestorRootNodes.forEach((node) => {
@@ -204,9 +208,11 @@ export const PositionMixin = (superClass) =>
     /** @private */
     __onScroll(e) {
       // If the scroll event occurred inside the overlay, ignore it.
-      if (!this.contains(e.target)) {
-        this._updatePosition();
+      if (e.target instanceof Node && this.contains(e.target)) {
+        return;
       }
+
+      this._updatePosition();
     }
 
     _updatePosition() {
diff --git a/packages/overlay/test/position-mixin-listeners.test.js b/packages/overlay/test/position-mixin-listeners.test.js
index 0eb0587094..5c6431feb2 100644
--- a/packages/overlay/test/position-mixin-listeners.test.js
+++ b/packages/overlay/test/position-mixin-listeners.test.js
@@ -68,8 +68,8 @@ describe('position mixin listeners', () => {
       updatePositionSpy.resetHistory();
     });
 
-    it('should not update position on resize', () => {
-      resize(window);
+    it('should not update position on visual viewport resize', () => {
+      resize(window.visualViewport);
       expect(updatePositionSpy.called).to.be.false;
     });
 
@@ -84,17 +84,17 @@ describe('position mixin listeners', () => {
       expect(updatePositionSpy.called).to.be.false;
     });
 
-    it('should update position on resize after assigning a position target', () => {
+    it('should update position on visual viewport resize after assigning a position target', () => {
       overlay.positionTarget = target;
       updatePositionSpy.resetHistory();
-      resize(window);
+      resize(window.visualViewport);
       expect(updatePositionSpy.called).to.be.true;
     });
 
-    it('should update position on document scroll after assigning a position target', () => {
+    it('should update position on visual viewport scroll after assigning a position target', () => {
       overlay.positionTarget = target;
       updatePositionSpy.resetHistory();
-      scroll(document);
+      scroll(window.visualViewport);
       expect(updatePositionSpy.called).to.be.true;
     });
 
@@ -126,14 +126,35 @@ describe('position mixin listeners', () => {
       updatePositionSpy.resetHistory();
     });
 
-    it('should update position on resize', () => {
+    it('should not update position on window resize', () => {
       resize(window);
+      expect(updatePositionSpy.called).to.be.false;
+    });
+
+    it('should not update position on document scroll', () => {
+      scroll(document);
+      expect(updatePositionSpy.called).to.be.false;
+    });
+
+    it('should update position on visual viewport resize', () => {
+      resize(window.visualViewport);
       expect(updatePositionSpy.called).to.be.true;
     });
 
-    it('should not update position on resize when closed', () => {
+    it('should not update position on visual viewport resize when closed', () => {
       overlay.opened = false;
-      resize(window);
+      resize(window.visualViewport);
+      expect(updatePositionSpy.called).to.be.false;
+    });
+
+    it('should update position on visual viewport scroll', () => {
+      scroll(window.visualViewport);
+      expect(updatePositionSpy.called).to.be.true;
+    });
+
+    it('should not update position on visual viewport scroll when closed', () => {
+      overlay.opened = false;
+      scroll(window.visualViewport);
       expect(updatePositionSpy.called).to.be.false;
     });
 
@@ -150,13 +171,13 @@ describe('position mixin listeners', () => {
       expect(updatePositionSpy.called).to.be.false;
     });
 
-    ['document', 'ancestor'].forEach((name) => {
+    ['visual viewport', 'ancestor'].forEach((name) => {
       describe(name, () => {
         let scrollableNode;
 
         beforeEach(() => {
-          if (name === 'document') {
-            scrollableNode = document;
+          if (name === 'visual viewport') {
+            scrollableNode = window.visualViewport;
           }
           if (name === 'ancestor') {
             scrollableNode = wrapper.shadowRoot.querySelector('#scrollable');
@@ -208,8 +229,8 @@ describe('position mixin listeners', () => {
         updatePositionSpy.resetHistory();
       });
 
-      it('should update position on document scroll', () => {
-        scroll(document);
+      it('should update position on visual viewport scroll', () => {
+        scroll(window.visualViewport);
         expect(updatePositionSpy.called).to.be.true;
       });
 
@@ -234,8 +255,8 @@ describe('position mixin listeners', () => {
         newWrapper.appendChild(target);
       });
 
-      it('should update position on document scroll after re-opened', async () => {
-        scroll(document);
+      it('should update position on visual viewport scroll after re-opened', async () => {
+        scroll(window.visualViewport);
         expect(updatePositionSpy.called).to.be.true;
 
         overlay.opened = false;
@@ -243,7 +264,7 @@ describe('position mixin listeners', () => {
         await nextFrame();
         updatePositionSpy.resetHistory();
 
-        scroll(document);
+        scroll(window.visualViewport);
         expect(updatePositionSpy.called).to.be.true;
       });