diff --git a/src/Cell.tsx b/src/Cell.tsx
index 82b0ee7bd2..d0a26f28bd 100644
--- a/src/Cell.tsx
+++ b/src/Cell.tsx
@@ -33,7 +33,6 @@ function Cell<R, SR>({
   isDraggedOver,
   row,
   rowIdx,
-  dragHandle,
   onClick,
   onDoubleClick,
   onContextMenu,
@@ -112,7 +111,6 @@ function Cell<R, SR>({
         tabIndex: childTabIndex,
         onRowChange: handleRowChange
       })}
-      {dragHandle}
     </div>
   );
 }
diff --git a/src/DataGrid.tsx b/src/DataGrid.tsx
index 70cc37ce31..1d7b31b609 100644
--- a/src/DataGrid.tsx
+++ b/src/DataGrid.tsx
@@ -799,13 +799,18 @@ function DataGrid<R, SR, K extends Key>(
     return isDraggedOver ? selectedPosition.idx : undefined;
   }
 
-  function getDragHandle(rowIdx: number) {
-    if (selectedPosition.rowIdx !== rowIdx || selectedPosition.mode === 'EDIT' || onFill == null) {
+  function renderDragHandle() {
+    if (
+      onFill == null ||
+      selectedPosition.mode === 'EDIT' ||
+      !isCellWithinViewportBounds(selectedPosition)
+    ) {
       return;
     }
 
     return (
       <DragHandle
+        gridRowStart={headerAndTopSummaryRowsCount + selectedPosition.rowIdx + 1}
         rows={rows}
         columns={columns}
         selectedPosition={selectedPosition}
@@ -952,7 +957,6 @@ function DataGrid<R, SR, K extends Key>(
           lastFrozenColumnIndex,
           onRowChange: handleFormatterRowChangeLatest,
           selectCell: selectCellLatest,
-          selectedCellDragHandle: getDragHandle(rowIdx),
           selectedCellEditor: getCellEditor(rowIdx)
         })
       );
@@ -1121,6 +1125,8 @@ function DataGrid<R, SR, K extends Key>(
         </RowSelectionChangeProvider>
       </DataGridDefaultRenderersProvider>
 
+      {renderDragHandle()}
+
       {/* render empty cells that span only 1 column so we can safely measure column widths, regardless of colSpan */}
       {renderMeasuringCells(viewportColumns)}
 
diff --git a/src/DragHandle.tsx b/src/DragHandle.tsx
index 2258aaf654..05d575bb4c 100644
--- a/src/DragHandle.tsx
+++ b/src/DragHandle.tsx
@@ -1,30 +1,39 @@
 import { css } from '@linaria/core';
+import clsx from 'clsx';
 
+import { getCellStyle } from './utils';
 import type { CalculatedColumn, FillEvent, Position } from './types';
 import type { DataGridProps, SelectCellState } from './DataGrid';
 
 const cellDragHandle = css`
   @layer rdg.DragHandle {
+    --rdg-drag-handle-size: 8px;
+    z-index: 0;
     cursor: move;
-    position: absolute;
-    inset-inline-end: 0;
-    inset-block-end: 0;
-    inline-size: 8px;
-    block-size: 8px;
+    inline-size: var(--rdg-drag-handle-size);
+    block-size: var(--rdg-drag-handle-size);
     background-color: var(--rdg-selection-color);
+    place-self: end;
 
     &:hover {
-      inline-size: 16px;
-      block-size: 16px;
+      --rdg-drag-handle-size: 16px;
       border: 2px solid var(--rdg-selection-color);
       background-color: var(--rdg-background-color);
     }
   }
 `;
 
+const cellDragHandleFrozenClassname = css`
+  @layer rdg.DragHandle {
+    z-index: 1;
+    position: sticky;
+  }
+`;
+
 const cellDragHandleClassname = `rdg-cell-drag-handle ${cellDragHandle}`;
 
 interface Props<R, SR> extends Pick<DataGridProps<R, SR>, 'rows' | 'onRowsChange'> {
+  gridRowStart: number;
   columns: readonly CalculatedColumn<R, SR>[];
   selectedPosition: SelectCellState;
   latestDraggedOverRowIdx: React.MutableRefObject<number | undefined>;
@@ -35,6 +44,7 @@ interface Props<R, SR> extends Pick<DataGridProps<R, SR>, 'rows' | 'onRowsChange
 }
 
 export default function DragHandle<R, SR>({
+  gridRowStart,
   rows,
   columns,
   selectedPosition,
@@ -45,6 +55,9 @@ export default function DragHandle<R, SR>({
   setDragging,
   setDraggedOverRowIdx
 }: Props<R, SR>) {
+  const { idx, rowIdx } = selectedPosition;
+  const column = columns[idx];
+
   function handleMouseDown(event: React.MouseEvent<HTMLDivElement>) {
     if (event.buttons !== 1) return;
     setDragging(true);
@@ -70,7 +83,6 @@ export default function DragHandle<R, SR>({
     const overRowIdx = latestDraggedOverRowIdx.current;
     if (overRowIdx === undefined) return;
 
-    const { rowIdx } = selectedPosition;
     const startRowIndex = rowIdx < overRowIdx ? rowIdx + 1 : overRowIdx;
     const endRowIndex = rowIdx < overRowIdx ? overRowIdx + 1 : rowIdx;
     updateRows(startRowIndex, endRowIndex);
@@ -79,11 +91,10 @@ export default function DragHandle<R, SR>({
 
   function handleDoubleClick(event: React.MouseEvent<HTMLDivElement>) {
     event.stopPropagation();
-    updateRows(selectedPosition.rowIdx + 1, rows.length);
+    updateRows(rowIdx + 1, rows.length);
   }
 
   function updateRows(startRowIdx: number, endRowIdx: number) {
-    const { idx, rowIdx } = selectedPosition;
     const column = columns[idx];
     const sourceRow = rows[rowIdx];
     const updatedRows = [...rows];
@@ -103,9 +114,20 @@ export default function DragHandle<R, SR>({
     }
   }
 
+  const colSpan = column.colSpan?.({ type: 'ROW', row: rows[rowIdx] }) ?? 1;
+  const style = getCellStyle(column, colSpan);
+
   return (
     <div
-      className={cellDragHandleClassname}
+      style={{
+        ...style,
+        gridRowStart,
+        insetInlineStart:
+          style.insetInlineStart && typeof column.width === 'number'
+            ? `calc(${style.insetInlineStart} + ${column.width}px - var(--rdg-drag-handle-size))`
+            : undefined
+      }}
+      className={clsx(cellDragHandleClassname, column.frozen && cellDragHandleFrozenClassname)}
       onMouseDown={handleMouseDown}
       onDoubleClick={handleDoubleClick}
     />
diff --git a/src/Row.tsx b/src/Row.tsx
index 7e4affbe9c..aab22bda6b 100644
--- a/src/Row.tsx
+++ b/src/Row.tsx
@@ -21,7 +21,6 @@ function Row<R, SR>(
     row,
     viewportColumns,
     selectedCellEditor,
-    selectedCellDragHandle,
     onCellClick,
     onCellDoubleClick,
     onCellContextMenu,
@@ -78,7 +77,6 @@ function Row<R, SR>(
           isCopied={copiedCellIdx === idx}
           isDraggedOver={draggedOverCellIdx === idx}
           isCellSelected={isCellSelected}
-          dragHandle={isCellSelected ? selectedCellDragHandle : undefined}
           onClick={onCellClick}
           onDoubleClick={onCellDoubleClick}
           onContextMenu={onCellContextMenu}
diff --git a/src/TreeDataGrid.tsx b/src/TreeDataGrid.tsx
index 7f8f151c27..8ee7675d8f 100644
--- a/src/TreeDataGrid.tsx
+++ b/src/TreeDataGrid.tsx
@@ -363,7 +363,6 @@ function TreeDataGrid<R, SR, K extends Key>(
       draggedOverCellIdx,
       setDraggedOverRowIdx,
       selectedCellEditor,
-      selectedCellDragHandle,
       ...rowProps
     }: RenderRowProps<R, SR>
   ) {
@@ -402,8 +401,7 @@ function TreeDataGrid<R, SR, K extends Key>(
       copiedCellIdx,
       draggedOverCellIdx,
       setDraggedOverRowIdx,
-      selectedCellEditor,
-      selectedCellDragHandle
+      selectedCellEditor
     });
   }
 
diff --git a/src/types.ts b/src/types.ts
index 14b7656c2b..2bb18ffa11 100644
--- a/src/types.ts
+++ b/src/types.ts
@@ -148,7 +148,6 @@ export interface CellRendererProps<TRow, TSummaryRow>
   isCopied: boolean;
   isDraggedOver: boolean;
   isCellSelected: boolean;
-  dragHandle: ReactElement<React.HTMLAttributes<HTMLDivElement>> | undefined;
   onClick: RenderRowProps<TRow, TSummaryRow>['onCellClick'];
   onDoubleClick: RenderRowProps<TRow, TSummaryRow>['onCellDoubleClick'];
   onContextMenu: RenderRowProps<TRow, TSummaryRow>['onCellContextMenu'];
@@ -213,7 +212,6 @@ export interface RenderRowProps<TRow, TSummaryRow = unknown>
   copiedCellIdx: number | undefined;
   draggedOverCellIdx: number | undefined;
   selectedCellEditor: ReactElement<RenderEditCellProps<TRow>> | undefined;
-  selectedCellDragHandle: ReactElement<React.HTMLAttributes<HTMLDivElement>> | undefined;
   onRowChange: (column: CalculatedColumn<TRow, TSummaryRow>, rowIdx: number, newRow: TRow) => void;
   rowClass: Maybe<(row: TRow, rowIdx: number) => Maybe<string>>;
   setDraggedOverRowIdx: ((overRowIdx: number) => void) | undefined;