diff --git a/packages/dashboard/src/vaadin-dashboard-widget.js b/packages/dashboard/src/vaadin-dashboard-widget.js
index 6a15e52e5e..2019c87e38 100644
--- a/packages/dashboard/src/vaadin-dashboard-widget.js
+++ b/packages/dashboard/src/vaadin-dashboard-widget.js
@@ -54,7 +54,7 @@ class DashboardWidget extends ControllerMixin(ElementMixin(PolylitMixin(LitEleme
           display: var(--_vaadin-dashboard-widget-actions-display, none);
           position: absolute;
           bottom: 0;
-          right: 0;
+          inset-inline-end: 0;
           font-size: 30px;
           cursor: grab;
           line-height: 1;
@@ -64,6 +64,10 @@ class DashboardWidget extends ControllerMixin(ElementMixin(PolylitMixin(LitEleme
           content: '\\2921';
         }
 
+        :host([dir='rtl']) #resize-handle::before {
+          content: '\\2922';
+        }
+
         :host::after {
           content: '';
           z-index: 2;
diff --git a/packages/dashboard/src/widget-resize-controller.js b/packages/dashboard/src/widget-resize-controller.js
index a720a83e2a..f05919a893 100644
--- a/packages/dashboard/src/widget-resize-controller.js
+++ b/packages/dashboard/src/widget-resize-controller.js
@@ -62,7 +62,7 @@ export class WidgetResizeController extends EventTarget {
       return;
     }
 
-    this.__resizeWidth = this.__resizeStartWidth + e.detail.dx;
+    this.__resizeWidth = this.__resizeStartWidth + (document.dir === 'rtl' ? -e.detail.dx : e.detail.dx);
     this.__resizeHeight = this.__resizeStartHeight + e.detail.dy;
     this.__updateWidgetStyles();
 
diff --git a/packages/dashboard/test/dashboard-widget-resizing.test.ts b/packages/dashboard/test/dashboard-widget-resizing.test.ts
index 28bb344a49..72e5982608 100644
--- a/packages/dashboard/test/dashboard-widget-resizing.test.ts
+++ b/packages/dashboard/test/dashboard-widget-resizing.test.ts
@@ -5,6 +5,7 @@ import '../vaadin-dashboard.js';
 import { isSafari } from '@vaadin/component-base/src/browser-utils.js';
 import type { Dashboard, DashboardItem } from '../vaadin-dashboard.js';
 import {
+  describeBidirectional,
   expectLayout,
   fireResizeEnd,
   fireResizeOver,
@@ -51,89 +52,91 @@ describe('dashboard - widget resizing', () => {
   });
 
   describe('mouse drag', () => {
-    it('should resize a widget while dragging (start -> end)', async () => {
-      // Start dragging the first widget resize handle
-      fireResizeStart(getElementFromCell(dashboard, 0, 0)!);
-      await nextFrame();
+    describeBidirectional('horizontal', () => {
+      it('should resize a widget while dragging (start -> end)', async () => {
+        // Start dragging the first widget resize handle
+        fireResizeStart(getElementFromCell(dashboard, 0, 0)!);
+        await nextFrame();
 
-      // Drag over the end edge of the second one
-      fireResizeOver(getElementFromCell(dashboard, 0, 1)!, 'end');
-      await nextFrame();
+        // Drag over the end edge of the second one
+        fireResizeOver(getElementFromCell(dashboard, 0, 1)!, 'end');
+        await nextFrame();
 
-      fireResizeEnd(dashboard);
-      await nextFrame();
+        fireResizeEnd(dashboard);
+        await nextFrame();
 
-      // Expect the widgets to be reordered
-      // prettier-ignore
-      expectLayout(dashboard, [
-        [0, 0],
-        [1],
-      ]);
-    });
+        // Expect the widgets to be reordered
+        // prettier-ignore
+        expectLayout(dashboard, [
+          [0, 0],
+          [1],
+        ]);
+      });
 
-    it('should not resize if dragged barely over another widget (start -> end)', async () => {
-      fireResizeStart(getElementFromCell(dashboard, 0, 0)!);
-      await nextFrame();
+      it('should not resize if dragged barely over another widget (start -> end)', async () => {
+        fireResizeStart(getElementFromCell(dashboard, 0, 0)!);
+        await nextFrame();
 
-      fireResizeOver(getElementFromCell(dashboard, 0, 1)!, 'start');
-      await nextFrame();
+        fireResizeOver(getElementFromCell(dashboard, 0, 1)!, 'start');
+        await nextFrame();
 
-      fireResizeEnd(dashboard);
-      await nextFrame();
+        fireResizeEnd(dashboard);
+        await nextFrame();
 
-      // prettier-ignore
-      expectLayout(dashboard, [
-        [0, 1],
-      ]);
-    });
+        // prettier-ignore
+        expectLayout(dashboard, [
+          [0, 1],
+        ]);
+      });
 
-    it('should resize a widget while dragging (end -> start)', async () => {
-      dashboard.items = [{ id: 0, colspan: 2 }, { id: 1 }];
-      await nextFrame();
-      // prettier-ignore
-      expectLayout(dashboard, [
-        [0, 0],
-        [1],
-      ]);
+      it('should resize a widget while dragging (end -> start)', async () => {
+        dashboard.items = [{ id: 0, colspan: 2 }, { id: 1 }];
+        await nextFrame();
+        // prettier-ignore
+        expectLayout(dashboard, [
+          [0, 0],
+          [1],
+        ]);
 
-      fireResizeStart(getElementFromCell(dashboard, 0, 1)!);
-      await nextFrame();
+        fireResizeStart(getElementFromCell(dashboard, 0, 1)!);
+        await nextFrame();
 
-      fireResizeOver(getElementFromCell(dashboard, 0, 0)!, 'start');
-      await nextFrame();
+        fireResizeOver(getElementFromCell(dashboard, 0, 0)!, 'start');
+        await nextFrame();
 
-      fireResizeEnd(dashboard);
-      await nextFrame();
+        fireResizeEnd(dashboard);
+        await nextFrame();
 
-      // prettier-ignore
-      expectLayout(dashboard, [
-        [0, 1],
-      ]);
-    });
+        // prettier-ignore
+        expectLayout(dashboard, [
+          [0, 1],
+        ]);
+      });
 
-    it('should not resize if dragged barely over another widget (end -> start)', async () => {
-      dashboard.items = [{ id: 0, colspan: 2 }, { id: 1 }];
-      await nextFrame();
-      // prettier-ignore
-      expectLayout(dashboard, [
-        [0, 0],
-        [1],
-      ]);
+      it('should not resize if dragged barely over another widget (end -> start)', async () => {
+        dashboard.items = [{ id: 0, colspan: 2 }, { id: 1 }];
+        await nextFrame();
+        // prettier-ignore
+        expectLayout(dashboard, [
+          [0, 0],
+          [1],
+        ]);
 
-      fireResizeStart(getElementFromCell(dashboard, 0, 1)!);
-      await nextFrame();
+        fireResizeStart(getElementFromCell(dashboard, 0, 1)!);
+        await nextFrame();
 
-      fireResizeOver(getElementFromCell(dashboard, 0, 0)!, 'end');
-      await nextFrame();
+        fireResizeOver(getElementFromCell(dashboard, 0, 0)!, 'end');
+        await nextFrame();
 
-      fireResizeEnd(dashboard);
-      await nextFrame();
+        fireResizeEnd(dashboard);
+        await nextFrame();
 
-      // prettier-ignore
-      expectLayout(dashboard, [
-        [0, 0],
-        [1],
-      ]);
+        // prettier-ignore
+        expectLayout(dashboard, [
+          [0, 0],
+          [1],
+        ]);
+      });
     });
 
     it('should resize a widget while dragging (top -> bottom)', async () => {
diff --git a/packages/dashboard/test/helpers.ts b/packages/dashboard/test/helpers.ts
index a3c59c48ba..e953e9b7da 100644
--- a/packages/dashboard/test/helpers.ts
+++ b/packages/dashboard/test/helpers.ts
@@ -37,13 +37,15 @@ function _getRowHeights(dashboard: Element): number[] {
 }
 
 function _getElementFromCell(dashboard: HTMLElement, rowIndex: number, columnIndex: number, rowHeights: number[]) {
-  const { top, left } = dashboard.getBoundingClientRect();
+  const { top, left, right } = dashboard.getBoundingClientRect();
   const columnWidths = getColumnWidths(dashboard);
-  const x = left + columnWidths.slice(0, columnIndex).reduce((sum, width) => sum + width, 0);
+  const columnOffset = columnWidths.slice(0, columnIndex).reduce((sum, width) => sum + width, 0);
+  const rtl = document.dir === 'rtl';
+  const x = rtl ? right - columnOffset : left + columnOffset;
   const y = top + rowHeights.slice(0, rowIndex).reduce((sum, height) => sum + height, 0);
 
   return document
-    .elementsFromPoint(x + columnWidths[columnIndex] / 2, y + rowHeights[rowIndex] - 1)
+    .elementsFromPoint(x + (columnWidths[columnIndex] / 2) * (rtl ? -1 : 1), y + rowHeights[rowIndex] - 1)
     .reverse()
     .find(
       (element) =>
@@ -279,3 +281,18 @@ export function fireResizeEnd(dragOverTarget: Element): void {
 export function getRemoveButton(section: DashboardWidget | DashboardSection): HTMLElement {
   return section.shadowRoot!.querySelector('#remove-button') as HTMLElement;
 }
+
+export function describeBidirectional(name: string, tests: () => void): void {
+  describe(name, tests);
+  describe(`${name} (RTL)`, () => {
+    before(() => {
+      document.dir = 'rtl';
+    });
+
+    after(() => {
+      document.dir = 'ltr'; // Reset to default after tests
+    });
+
+    tests();
+  });
+}