diff --git a/packages/@react-spectrum/s2/src/TableView.tsx b/packages/@react-spectrum/s2/src/TableView.tsx
index 1737a6c5549..220629c6f92 100644
--- a/packages/@react-spectrum/s2/src/TableView.tsx
+++ b/packages/@react-spectrum/s2/src/TableView.tsx
@@ -94,7 +94,7 @@ import {GridNode} from 'react-stately/private/grid/GridCollection';
 import {IconContext} from './Icon';
 import intlMessages from '../intl/*.json';
 import {Key} from '@react-types/shared';
-import {LayoutInfo, Rect, TableLayout, Virtualizer} from 'react-aria-components/Virtualizer';
+import {LayoutInfo, TableLayout, Virtualizer} from 'react-aria-components/Virtualizer';
 import {LayoutNode} from 'react-stately/useVirtualizerState';
 import {Menu, MenuItem, MenuSection, MenuTrigger} from './Menu';
 import Nubbin from '../ui-icons/S2_MoveHorizontalTableWidget.svg';
@@ -257,6 +257,8 @@ const table = style<
   minWidth: 0,
   fontFamily: 'sans',
   fontWeight: 'normal',
+  display: 'flex',
+  flexDirection: 'column',
   overflow: 'auto',
   backgroundColor: {
     default: 'gray-25',
@@ -343,13 +345,6 @@ export class S2TableLayout<T> extends TableLayout<T> {
     if (rowGroups.length < 2) {
       return [];
     }
-    let {layoutInfo} = rowGroups[1];
-    // TableLayout's buildCollection always sets the body width to the max width between the header width, but
-    // we want the body to be sticky and only as wide as the table so it is always in view if loading/empty
-    let isEmptyOrLoading = this.virtualizer?.collection.size === 0;
-    if (isEmptyOrLoading) {
-      layoutInfo.rect.width = this.virtualizer!.size.width - 80;
-    }
 
     return rowGroups;
   }
@@ -359,11 +354,6 @@ export class S2TableLayout<T> extends TableLayout<T> {
     let {layoutInfo} = layoutNode;
     layoutInfo.allowOverflow = true;
     layoutInfo.rect.width = this.virtualizer!.size.width;
-    // If performing first load or empty, the body will be sticky so we don't want to apply sticky to the loader, otherwise it will
-    // affect the positioning of the empty state renderer
-    let collection = this.virtualizer!.collection;
-    let isEmptyOrLoading = collection?.size === 0;
-    layoutInfo.isSticky = !isEmptyOrLoading;
     return layoutNode;
   }
 
@@ -375,16 +365,15 @@ export class S2TableLayout<T> extends TableLayout<T> {
     let {layoutInfo} = layoutNode;
     // Needs overflow for sticky loader
     layoutInfo.allowOverflow = true;
-    // If loading or empty, we'll want the body to be sticky and centered
+    // The base TableLayout.buildRowGroup sizes the empty/loading body from the virtualizer's
+    // current on-screen size, which is circular when no explicit height is set (the empty-state
+    // content is rendered outside this virtualized rect entirely, see Table.tsx's TableInner).
+    // Reset it back to the real (near-zero) computed height so it doesn't feed back into the
+    // ResizeObserver that measures that same on-screen size.
     let isEmptyOrLoading = this.virtualizer?.collection.size === 0;
     if (isEmptyOrLoading) {
-      layoutInfo.rect = new Rect(
-        40,
-        40,
-        this.virtualizer!.size.width - 80,
-        this.virtualizer!.size.height - 80
-      );
-      layoutInfo.isSticky = true;
+      let maxY = layoutNode.children?.reduce((max, child) => Math.max(max, child.layoutInfo.rect.maxY), layoutInfo.rect.y) ?? layoutInfo.rect.y;
+      layoutInfo.rect.height = maxY - layoutInfo.rect.y;
     }
 
     return {...layoutNode, layoutInfo};
diff --git a/packages/@react-spectrum/s2/stories/TableView.stories.tsx b/packages/@react-spectrum/s2/stories/TableView.stories.tsx
index 3f4e1da7a65..b8d79b467d6 100644
--- a/packages/@react-spectrum/s2/stories/TableView.stories.tsx
+++ b/packages/@react-spectrum/s2/stories/TableView.stories.tsx
@@ -438,7 +438,7 @@ function renderEmptyState() {
 }
 
 const EmptyStateTable = (args: TableViewProps): ReactElement => (
-  <TableView aria-label="Empty state" {...args} styles={style({height: 320, width: 320})}>
+  <TableView aria-label="Empty state" {...args} styles={style({ width: 320})}>
     <TableHeader columns={columns}>
       {column => (
         <Column minWidth={200} width={200} isRowHeader={column.isRowHeader}>
@@ -459,6 +459,31 @@ export const EmptyState: StoryObj<typeof EmptyStateTable> = {
   }
 };
 
+// No explicit height set at all: https://github.com/adobe/react-spectrum/issues/10235
+// The table should still auto-size to show the column headers and the empty state.
+const EmptyStateTableNoHeight = (args: TableViewProps): ReactElement => (
+  <TableView aria-label="Empty state, no height" {...args} styles={style({width: 320})}>
+    <TableHeader columns={columns}>
+      {column => (
+        <Column minWidth={200} width={200} isRowHeader={column.isRowHeader}>
+          {column.name}
+        </Column>
+      )}
+    </TableHeader>
+    <TableBody items={[]} renderEmptyState={renderEmptyState}>
+      {[]}
+    </TableBody>
+  </TableView>
+);
+
+export const EmptyStateNoHeight: StoryObj<typeof EmptyStateTableNoHeight> = {
+  render: EmptyStateTableNoHeight,
+  args: {
+    ...Example.args
+  },
+  name: 'empty state, no explicit height'
+};
+
 export const LoadingStateNoItems: StoryObj<typeof EmptyStateTable> = {
   render: EmptyStateTable,
   args: {
diff --git a/packages/react-aria-components/src/Table.tsx b/packages/react-aria-components/src/Table.tsx
index 45eb1d488bf..a9f72fee678 100644
--- a/packages/react-aria-components/src/Table.tsx
+++ b/packages/react-aria-components/src/Table.tsx
@@ -888,6 +888,21 @@ function TableInner({props, forwardedRef: ref, selectionState, collection}: Tabl
 
   let DOMProps = filterDOMProps(props, {global: true});
 
+  let bodyNode = filteredState.collection.body;
+  let isBodyEmpty = filteredState.collection.size === 0;
+  let renderEmptyState = bodyNode?.props?.renderEmptyState;
+  let {rowGroupProps: emptyRowGroupProps} = useTableRowGroup();
+  let emptyStateRowGroup = isVirtualized && isBodyEmpty && renderEmptyState && (
+    <TableBodyElementType {...emptyRowGroupProps} data-empty="true">
+      {renderTableEmptyState(
+        renderEmptyState,
+        {isDropTarget: isRootDropTarget, isEmpty: isBodyEmpty},
+        filteredState.collection.columnCount,
+        isVirtualized
+      )}
+    </TableBodyElementType>
+  );
+
   return (
     <Provider
       values={[
@@ -921,6 +936,7 @@ function TableInner({props, forwardedRef: ref, selectionState, collection}: Tabl
               scrollRef={tableContainerContext?.scrollRef ?? ref}
               persistedKeys={useDndPersistedKeys(selectionManager, dragAndDropHooks, dropState)}
             />
+            {emptyStateRowGroup}
           </SharedElementTransition>
         </TableElementType>
       </FocusScope>
@@ -1500,6 +1516,31 @@ let TableBodyElementType = forwardRef(function TableBodyElementType(
   return <dom.tbody {...props} ref={ref} />;
 });
 
+function renderTableEmptyState(
+  renderEmptyState: (props: TableBodyRenderProps) => ReactNode,
+  renderValues: TableBodyRenderProps,
+  numColumns: number,
+  isVirtualized: boolean
+) {
+  let rowProps = {};
+  let rowHeaderProps = {};
+  let style = {};
+  if (isVirtualized) {
+    rowHeaderProps['aria-colspan'] = numColumns;
+    style = {display: 'contents'};
+  } else {
+    rowHeaderProps['colSpan'] = numColumns;
+  }
+
+  return (
+    <TableRowElementType role="row" {...rowProps} style={style}>
+      <TableCellElementType role="rowheader" {...rowHeaderProps} style={style}>
+        {renderEmptyState(renderValues)}
+      </TableCellElementType>
+    </TableRowElementType>
+  );
+}
+
 /**
  * The body of a `<Table>`, containing the table rows.
  */
@@ -1535,24 +1576,11 @@ export const TableBody = /*#__PURE__*/ createBranchComponent(
     let emptyState;
     let numColumns = collection.columnCount;
 
-    if (isEmpty && props.renderEmptyState && state) {
-      let rowProps = {};
-      let rowHeaderProps = {};
-      let style = {};
-      if (isVirtualized) {
-        rowHeaderProps['aria-colspan'] = numColumns;
-        style = {display: 'contents'};
-      } else {
-        rowHeaderProps['colSpan'] = numColumns;
-      }
-
-      emptyState = (
-        <TableRowElementType role="row" {...rowProps} style={style}>
-          <TableCellElementType role="rowheader" {...rowHeaderProps} style={style}>
-            {props.renderEmptyState(renderValues)}
-          </TableCellElementType>
-        </TableRowElementType>
-      );
+    // When virtualized, the empty state is rendered as a sibling of the CollectionRoot
+    // in TableInner instead, so that it can be sized by its own content rather than being
+    // trapped in a `contain: size` virtualizer-positioned box. See TableInner.
+    if (!isVirtualized && isEmpty && props.renderEmptyState && state) {
+      emptyState = renderTableEmptyState(props.renderEmptyState, renderValues, numColumns, isVirtualized);
     }
 
     let {rowGroupProps} = useTableRowGroup();