diff --git a/MIGRATION.md b/MIGRATION.md
index 0805c3682b8b..2b6ba2137b9c 100644
--- a/MIGRATION.md
+++ b/MIGRATION.md
@@ -627,6 +627,16 @@ The PopoverProvider component acts as a counterpoint to WithTooltip. When you wa
 
 PopoverProvider is based on react-aria. It must have a single child that acts as a trigger. This child must have a pressable role (can be clicked or pressed) and must be able to receive React refs. Wrap your trigger component in `forwardRef` if you notice placement issues for your popover.
 
+##### Added: ariaLabel
+
+The `ariaLabel` prop was added in Storybook 10.3 to provide an accessible label for the popover dialog. This label is announced by screen readers when the popover opens. `ariaLabel` will become mandatory in Storybook 11.
+
+```tsx
+<PopoverProvider ariaLabel="Share options" popover={<ShareMenu />}>
+  <Button ariaLabel="Share">Share</Button>
+</PopoverProvider>
+```
+
 #### WithTooltip Component API Changes
 
 The WithTooltip component has been reimplemented from the ground up, under the new name `TooltipProvider`. The new implementation will replace `WithTooltip` entirely in Storybook 11. Below is a summary of the changes between both APIs, which will take full effect in Storybook 11.
diff --git a/code/addons/docs/src/blocks/components/ArgsTable/ArgValue.tsx b/code/addons/docs/src/blocks/components/ArgsTable/ArgValue.tsx
index 1be3d2075744..66a723c592ad 100644
--- a/code/addons/docs/src/blocks/components/ArgsTable/ArgValue.tsx
+++ b/code/addons/docs/src/blocks/components/ArgsTable/ArgValue.tsx
@@ -203,6 +203,7 @@ const ArgSummary: FC<ArgSummaryProps> = ({ value, initialExpandedArgs }) => {
 
   return (
     <PopoverProvider
+      ariaLabel="Arg value details"
       placement="bottom"
       visible={isOpen}
       onVisibleChange={(isVisible) => {
diff --git a/code/addons/docs/src/blocks/controls/Color.tsx b/code/addons/docs/src/blocks/controls/Color.tsx
index 3c3610c21621..0758f7b8611c 100644
--- a/code/addons/docs/src/blocks/controls/Color.tsx
+++ b/code/addons/docs/src/blocks/controls/Color.tsx
@@ -393,6 +393,7 @@ export const ColorControl: FC<ColorControlProps> = ({
         placeholder="Choose color..."
       />
       <PopoverProvider
+        ariaLabel="Color picker"
         defaultVisible={startOpen}
         visible={readOnly ? false : undefined}
         onVisibleChange={() => color && addPreset(color)}
diff --git a/code/core/src/components/components/Popover/PopoverProvider.stories.tsx b/code/core/src/components/components/Popover/PopoverProvider.stories.tsx
index c6a4f4f68cb5..0db176a23c44 100644
--- a/code/core/src/components/components/Popover/PopoverProvider.stories.tsx
+++ b/code/core/src/components/components/Popover/PopoverProvider.stories.tsx
@@ -28,6 +28,7 @@ const meta = preview.meta({
   title: 'Overlay/PopoverProvider',
   component: PopoverProvider,
   args: {
+    ariaLabel: 'Sample popover',
     hasChrome: true,
     offset: 8,
     placement: 'top',
diff --git a/code/core/src/components/components/Popover/PopoverProvider.tsx b/code/core/src/components/components/Popover/PopoverProvider.tsx
index 7b953613c32a..d597c8d0f494 100644
--- a/code/core/src/components/components/Popover/PopoverProvider.tsx
+++ b/code/core/src/components/components/Popover/PopoverProvider.tsx
@@ -1,5 +1,7 @@
 import type { DOMAttributes, ReactElement, ReactNode } from 'react';
-import React, { useCallback, useState } from 'react';
+import React, { cloneElement, useCallback, useState } from 'react';
+
+import { deprecate } from 'storybook/internal/client-logger';
 
 import { Pressable } from '@react-aria/interactions';
 import { DialogTrigger } from 'react-aria-components/patched-dist/Dialog';
@@ -9,6 +11,12 @@ import { type PopperPlacement, convertToReactAriaPlacement } from '../shared/ove
 import { Popover } from './Popover';
 
 export interface PopoverProviderProps {
+  /**
+   * An accessible label for the popover dialog, announced by screen readers. This prop will become
+   * mandatory in Storybook 11. Provide a concise description of the popover's purpose.
+   */
+  ariaLabel?: string;
+
   /** Whether to display the Popover in a prestyled container. True by default. */
   hasChrome?: boolean;
 
@@ -53,6 +61,7 @@ export interface PopoverProviderProps {
 }
 
 export const PopoverProvider = ({
+  ariaLabel,
   placement: placementProp = 'bottom-start',
   hasChrome = true,
   hasCloseButton = false,
@@ -66,6 +75,12 @@ export const PopoverProvider = ({
   onVisibleChange,
   ...props
 }: PopoverProviderProps) => {
+  if (!ariaLabel) {
+    deprecate(
+      "The 'ariaLabel' prop on 'PopoverProvider' will become mandatory in Storybook 11. Provide a concise, accessible label describing the popover's purpose."
+    );
+  }
+
   // Map Popper.js placement to react-aria placement best we can.
   const placement = convertToReactAriaPlacement(placementProp);
 
@@ -86,8 +101,22 @@ export const PopoverProvider = ({
       onOpenChange={onOpenChange}
       {...props}
     >
-      <Pressable>{children}</Pressable>
-      <PopoverUpstream placement={placement} offset={offset} style={{ outline: 'none' }}>
+      <Pressable>
+        {
+          /* React-aria does not inject aria-haspopup='dialog' to support legacy screen readers, so we do it ourselves. */
+          cloneElement(
+            children,
+            // @ts-expect-error aria-haspopup is a valid ARIA attribute but cloneElement types are too strict
+            { 'aria-haspopup': 'dialog' }
+          )
+        }
+      </Pressable>
+      <PopoverUpstream
+        aria-label={ariaLabel}
+        placement={placement}
+        offset={offset}
+        style={{ outline: 'none' }}
+      >
         <Popover
           hasChrome={hasChrome}
           hideLabel={closeLabel}
diff --git a/code/core/src/components/components/Tabs/Tabs.hooks.tsx b/code/core/src/components/components/Tabs/Tabs.hooks.tsx
index 4e834760b819..6113cfcf900c 100644
--- a/code/core/src/components/components/Tabs/Tabs.hooks.tsx
+++ b/code/core/src/components/components/Tabs/Tabs.hooks.tsx
@@ -69,6 +69,7 @@ export function useList(list: ChildrenListComplete) {
       return (
         <>
           <PopoverProvider
+            ariaLabel="Additional tabs"
             visible={isTooltipVisible}
             onVisibleChange={setTooltipVisible}
             placement="bottom"
diff --git a/code/core/src/components/components/tooltip/TooltipMessage.stories.tsx b/code/core/src/components/components/tooltip/TooltipMessage.stories.tsx
index e041453a94f6..9de23369b9a9 100644
--- a/code/core/src/components/components/tooltip/TooltipMessage.stories.tsx
+++ b/code/core/src/components/components/tooltip/TooltipMessage.stories.tsx
@@ -27,7 +27,13 @@ const WithPopoverDecorator: DecoratorFunction = (storyFn) => (
       height: '300px',
     }}
   >
-    <PopoverProvider placement="top" visible padding={0} popover={storyFn()}>
+    <PopoverProvider
+      ariaLabel="Tooltip message"
+      placement="top"
+      visible
+      padding={0}
+      popover={storyFn()}
+    >
       <Button ariaLabel={false}>Popover</Button>
     </PopoverProvider>
   </div>
diff --git a/code/core/src/manager/components/preview/tools/share.tsx b/code/core/src/manager/components/preview/tools/share.tsx
index caa46f7c78d4..63c688b0d4af 100644
--- a/code/core/src/manager/components/preview/tools/share.tsx
+++ b/code/core/src/manager/components/preview/tools/share.tsx
@@ -146,6 +146,7 @@ export const shareTool: Addon_BaseType = {
       {({ api, storyId, refId }) =>
         storyId ? (
           <PopoverProvider
+            ariaLabel="Share this story"
             hasChrome
             placement="bottom"
             padding={0}
diff --git a/code/core/src/manager/components/sidebar/ChecklistWidget.tsx b/code/core/src/manager/components/sidebar/ChecklistWidget.tsx
index 4712a89fb22f..b94251a92eac 100644
--- a/code/core/src/manager/components/sidebar/ChecklistWidget.tsx
+++ b/code/core/src/manager/components/sidebar/ChecklistWidget.tsx
@@ -247,7 +247,7 @@ export const ChecklistWidget = () => {
                   <CollapseToggle
                     {...toggleProps}
                     id="checklist-module-collapse-toggle"
-                    ariaLabel={`${isCollapsed ? 'Expand' : 'Collapse'} onboarding checklist`}
+                    ariaLabel={`${isCollapsed ? 'Expand' : 'Collapse'} onboarding guide`}
                   >
                     <ChevronSmallUpIcon
                       style={{
@@ -259,6 +259,7 @@ export const ChecklistWidget = () => {
                   </CollapseToggle>
                   {loaded && (
                     <PopoverProvider
+                      ariaLabel="Onboarding guide menu"
                       padding={0}
                       popover={({ onHide }) => (
                         <ActionList>
diff --git a/code/core/src/manager/components/sidebar/ContextMenu.tsx b/code/core/src/manager/components/sidebar/ContextMenu.tsx
index 55bd6b9f34da..93894cec3dd9 100644
--- a/code/core/src/manager/components/sidebar/ContextMenu.tsx
+++ b/code/core/src/manager/components/sidebar/ContextMenu.tsx
@@ -196,6 +196,7 @@ export const useContextMenu = (context: API_HashEntry, links: Link[], api: API)
       onMouseEnter: handlers.onMouseEnter,
       node: shouldRender ? (
         <PopoverProvider
+          ariaLabel="Context menu"
           placement="bottom-end"
           defaultVisible={false}
           visible={isOpen}
diff --git a/code/core/src/manager/components/sidebar/Menu.tsx b/code/core/src/manager/components/sidebar/Menu.tsx
index c5c75dc331f0..78bb673fe8a6 100644
--- a/code/core/src/manager/components/sidebar/Menu.tsx
+++ b/code/core/src/manager/components/sidebar/Menu.tsx
@@ -199,6 +199,7 @@ export const SidebarMenu: FC<SidebarMenuProps> = ({ menu, isHighlighted, onClick
 
   return (
     <PopoverProvider
+      ariaLabel="Storybook menu"
       placement={'bottom-start'}
       padding={0}
       popover={({ onHide }) => <SidebarMenuList onHide={onHide} menu={menu} />}
diff --git a/code/core/src/manager/components/sidebar/RefBlocks.tsx b/code/core/src/manager/components/sidebar/RefBlocks.tsx
index e908249eb068..9ef2564ab2e4 100644
--- a/code/core/src/manager/components/sidebar/RefBlocks.tsx
+++ b/code/core/src/manager/components/sidebar/RefBlocks.tsx
@@ -127,6 +127,7 @@ export const ErrorBlock: FC<{ error: Error }> = ({ error }) => {
           Oh no! Something went wrong loading this Storybook.
           <br />
           <PopoverProvider
+            ariaLabel="Error details"
             hasCloseButton
             offset={isMobile ? 0 : 8}
             placement={isMobile ? 'bottom-end' : 'bottom-start'}
diff --git a/code/core/src/manager/components/sidebar/RefIndicator.tsx b/code/core/src/manager/components/sidebar/RefIndicator.tsx
index 4d76d4f409ba..8c77da02dbb6 100644
--- a/code/core/src/manager/components/sidebar/RefIndicator.tsx
+++ b/code/core/src/manager/components/sidebar/RefIndicator.tsx
@@ -155,6 +155,7 @@ export const RefIndicator = React.memo(
       return (
         <IndicatorPlacement ref={forwardedRef}>
           <PopoverProvider
+            ariaLabel="Composed Storybook status"
             placement={isMobile ? 'bottom' : 'bottom-start'}
             padding={0}
             popover={() => (
diff --git a/code/core/src/manager/components/sidebar/TagsFilter.tsx b/code/core/src/manager/components/sidebar/TagsFilter.tsx
index 31d49b8c0e8f..6c8dd4667ba6 100644
--- a/code/core/src/manager/components/sidebar/TagsFilter.tsx
+++ b/code/core/src/manager/components/sidebar/TagsFilter.tsx
@@ -212,6 +212,7 @@ export const TagsFilter = ({ api, indexJson, tagPresets }: TagsFilterProps) => {
 
   return (
     <PopoverProvider
+      ariaLabel="Tag filters"
       placement="bottom"
       onVisibleChange={setExpanded}
       offset={8}
@@ -236,7 +237,6 @@ export const TagsFilter = ({ api, indexJson, tagPresets }: TagsFilterProps) => {
         key="tags"
         ariaLabel="Tag filters"
         ariaDescription="Filter the items shown in a sidebar based on the tags applied to them."
-        aria-haspopup="dialog"
         variant="ghost"
         padding="small"
         isHighlighted={tagsActive}
diff --git a/code/core/src/manager/container/Menu.stories.tsx b/code/core/src/manager/container/Menu.stories.tsx
index 5c81f339a7c9..0368fbf4d89a 100644
--- a/code/core/src/manager/container/Menu.stories.tsx
+++ b/code/core/src/manager/container/Menu.stories.tsx
@@ -21,7 +21,13 @@ export default {
           height: '300px',
         }}
       >
-        <PopoverProvider placement="top" defaultVisible padding={0} popover={storyFn()}>
+        <PopoverProvider
+          ariaLabel="Menu"
+          placement="top"
+          defaultVisible
+          padding={0}
+          popover={storyFn()}
+        >
           <Button ariaLabel={false}>Click me</Button>
         </PopoverProvider>
       </div>