diff --git a/src/autosuggest/__integ__/virtual-scroll.test.ts b/src/autosuggest/__integ__/virtual-scroll.test.ts
new file mode 100644
index 0000000000..7c3f4fd89f
--- /dev/null
+++ b/src/autosuggest/__integ__/virtual-scroll.test.ts
@@ -0,0 +1,73 @@
+// Copyright Amazon.com, Inc. or its affiliates. All Rights Reserved.
+// SPDX-License-Identifier: Apache-2.0
+import useBrowser from '@cloudscape-design/browser-test-tools/use-browser';
+
+import AutosuggestPage from './page-objects/autosuggest-page';
+
+class VirtualScrollAutosuggestPage extends AutosuggestPage {
+  listSelector = this.wrapper.findDropdown().findOptionsContainer().toSelector();
+
+  async wheelOverList(deltaY: number) {
+    // Wheel input is separate from the pointer, so this scrolls without hovering any option.
+    const list = await this.browser.$(this.listSelector);
+    await this.browser.action('wheel').scroll({ origin: list, deltaY, duration: 100 }).perform();
+  }
+
+  async getListScrollTop() {
+    const { top } = await this.getElementScroll(this.listSelector);
+    return top;
+  }
+}
+
+function setupTest(testFn: (page: VirtualScrollAutosuggestPage) => Promise<void>) {
+  return useBrowser(async browser => {
+    const page = new VirtualScrollAutosuggestPage(browser);
+    await browser.url('/#/light/autosuggest/virtual-scroll');
+    await page.focusInput();
+    await page.assertDropdownOpen();
+    await testFn(page);
+  });
+}
+
+describe('Autosuggest with virtual scroll', () => {
+  test(
+    'keeps the scroll position after wheel scrolling a dropdown opened with the mouse',
+    setupTest(async page => {
+      await page.wheelOverList(600);
+      await page.waitForJsTimers(100);
+      expect(await page.getListScrollTop()).toBeGreaterThan(0);
+
+      const scrollTop = await page.getListScrollTop();
+      await page.wheelOverList(600);
+      await page.waitForJsTimers(100);
+      expect(await page.getListScrollTop()).toBeGreaterThan(scrollTop);
+    })
+  );
+
+  test(
+    'keeps the scroll position after keyboard navigation when the list is scrolled without the wheel',
+    setupTest(async page => {
+      await page.keys(['ArrowDown', 'ArrowDown']);
+      await page.assertHighlightedOptionContains('Option 2');
+
+      // Stands in for dragging the scrollbar.
+      await page.elementScrollTo(page.listSelector, { top: 3000 });
+      await page.waitForJsTimers(100);
+      // The virtualizer shifts the offset slightly once it measures the newly rendered options,
+      // so don't expect exactly 3000. Without the fix the list snaps back to the highlighted option at the top.
+      expect(await page.getListScrollTop()).toBeGreaterThan(2500);
+    })
+  );
+
+  test(
+    'scrolls the highlighted option into view on keyboard navigation after the list was scrolled',
+    setupTest(async page => {
+      await page.elementScrollTo(page.listSelector, { top: 3000 });
+      await page.waitForJsTimers(100);
+
+      await page.keys(['ArrowDown']);
+      await page.assertHighlightedOptionContains('Option 1');
+      await page.waitForAssertion(async () => expect(await page.getListScrollTop()).toBe(0));
+    })
+  );
+});
diff --git a/src/autosuggest/virtual-list.tsx b/src/autosuggest/virtual-list.tsx
index a4e7671fbb..e0be769817 100644
--- a/src/autosuggest/virtual-list.tsx
+++ b/src/autosuggest/virtual-list.tsx
@@ -3,6 +3,7 @@
 import React, { useCallback, useEffect, useImperativeHandle, useRef } from 'react';
 
 import { useContainerQuery } from '@cloudscape-design/component-toolkit';
+import { useStableCallback } from '@cloudscape-design/component-toolkit/internal';
 
 import OptionsList from '../internal/components/options-list';
 import { useVirtual } from '../internal/hooks/use-virtual';
@@ -28,7 +29,7 @@ const VirtualList = ({
   const [width, strutRef] = useContainerQuery(rect => rect.contentBoxWidth, []);
   useImperativeHandle(strutRef, () => scrollRef.current);
 
-  const rowVirtualizer = useVirtual({
+  const { virtualItems, totalSize, scrollToIndex } = useVirtual({
     items: autosuggestItemsState.items,
     parentRef: scrollRef,
     // estimateSize is a dependency of measurements memo. We update it to force full recalculation
@@ -39,11 +40,21 @@ const VirtualList = ({
     estimateSize: useCallback(() => 31, [width, highlightText]),
   });
 
+  // Scroll when the highlight changes and moveFocus is true. The scrollToIndex identity changes
+  // whenever the number of items changes (e.g. when the next page of options is loaded), which
+  // shouldn't reset the scroll position either.
+  const scrollToHighlightedIndex = useStableCallback(scrollToIndex);
   useEffect(() => {
     if (autosuggestItemsState.highlightType.moveFocus) {
-      rowVirtualizer.scrollToIndex(autosuggestItemsState.highlightedIndex);
+      const index = autosuggestItemsState.highlightedIndex;
+      scrollToHighlightedIndex(index);
+      // Options are rendered with estimated sizes and measured afterwards, which can push the highlighted option out
+      // of view (e.g. when jumping to the last option). With React 18 the measurement happens after react-virtual's own
+      // retry, so retry once more after it.
+      const timeout = setTimeout(() => scrollToHighlightedIndex(index), 0);
+      return () => clearTimeout(timeout);
     }
-  }, [autosuggestItemsState.highlightType, autosuggestItemsState.highlightedIndex, rowVirtualizer]);
+  }, [autosuggestItemsState.highlightType, autosuggestItemsState.highlightedIndex, scrollToHighlightedIndex]);
 
   let lastGroupIndex = -1;
 
@@ -53,9 +64,9 @@ const VirtualList = ({
         aria-hidden="true"
         key="total-size"
         className={styles['layout-strut']}
-        style={{ height: rowVirtualizer.totalSize + (autosuggestItemsState.items.length === 1 ? 1 : 0) }}
+        style={{ height: totalSize + (autosuggestItemsState.items.length === 1 ? 1 : 0) }}
       />
-      {rowVirtualizer.virtualItems.map(virtualRow => {
+      {virtualItems.map(virtualRow => {
         const { index, start, measureRef } = virtualRow;
         const item = autosuggestItemsState.items[index];
         const optionProps = getOptionProps(