diff --git a/packages/ariakit/src/panel/PanelFileInput.tsx b/packages/ariakit/src/panel/PanelFileInput.tsx
index 12aef33147..29bc9560c5 100644
--- a/packages/ariakit/src/panel/PanelFileInput.tsx
+++ b/packages/ariakit/src/panel/PanelFileInput.tsx
@@ -4,22 +4,33 @@ import {
 } from "@ariakit/react";
 
 import { assertEmpty } from "@blocknote/core";
-import { ComponentProps } from "@blocknote/react";
+import { ComponentProps, useAutoFocus, useMergeRefs } from "@blocknote/react";
 import { forwardRef, type ChangeEvent } from "react";
 
 export const PanelFileInput = forwardRef<
   HTMLInputElement,
   ComponentProps["FilePanel"]["FileInput"]
 >((props, ref) => {
-  const { className, accept, value, placeholder, onChange, ...rest } = props;
+  const {
+    autoFocus,
+    className,
+    accept,
+    value,
+    placeholder,
+    onChange,
+    ...rest
+  } = props;
 
   assertEmpty(rest);
 
+  const inputRef = useAutoFocus<HTMLInputElement>(autoFocus);
+  const mergedRef = useMergeRefs([ref, inputRef]);
+
   return (
     <AriakitFormProvider>
       <AriakitFormInput
         className={className}
-        ref={ref}
+        ref={mergedRef}
         name={"panel-input"}
         type={"file"}
         accept={accept}
diff --git a/packages/ariakit/src/panel/PanelTextInput.tsx b/packages/ariakit/src/panel/PanelTextInput.tsx
index 91dd1a2394..51b444ca81 100644
--- a/packages/ariakit/src/panel/PanelTextInput.tsx
+++ b/packages/ariakit/src/panel/PanelTextInput.tsx
@@ -4,17 +4,28 @@ import {
 } from "@ariakit/react";
 
 import { assertEmpty, mergeCSSClasses } from "@blocknote/core";
-import { ComponentProps } from "@blocknote/react";
+import { ComponentProps, useAutoFocus, useMergeRefs } from "@blocknote/react";
 import { forwardRef } from "react";
 
 export const PanelTextInput = forwardRef<
   HTMLInputElement,
   ComponentProps["FilePanel"]["TextInput"]
 >((props, ref) => {
-  const { className, value, placeholder, onKeyDown, onChange, ...rest } = props;
+  const {
+    autoFocus,
+    className,
+    value,
+    placeholder,
+    onKeyDown,
+    onChange,
+    ...rest
+  } = props;
 
   assertEmpty(rest);
 
+  const inputRef = useAutoFocus<HTMLInputElement>(autoFocus);
+  const mergedRef = useMergeRefs([ref, inputRef]);
+
   return (
     <AriakitFormProvider>
       <AriakitFormInput
@@ -25,7 +36,7 @@ export const PanelTextInput = forwardRef<
         onChange={onChange}
         onKeyDown={onKeyDown}
         data-test={"embed-input"}
-        ref={ref}
+        ref={mergedRef}
       />
     </AriakitFormProvider>
   );
diff --git a/packages/mantine/src/panel/PanelFileInput.tsx b/packages/mantine/src/panel/PanelFileInput.tsx
index ed2efe8eb1..a1e5ae9ba2 100644
--- a/packages/mantine/src/panel/PanelFileInput.tsx
+++ b/packages/mantine/src/panel/PanelFileInput.tsx
@@ -1,22 +1,33 @@
 import { FileInput as MantineFileInput } from "@mantine/core";
 
 import { assertEmpty } from "@blocknote/core";
-import { ComponentProps } from "@blocknote/react";
+import { ComponentProps, useAutoFocus, useMergeRefs } from "@blocknote/react";
 import { forwardRef } from "react";
 
 export const PanelFileInput = forwardRef<
   HTMLButtonElement,
   ComponentProps["FilePanel"]["FileInput"]
 >((props, ref) => {
-  const { className, accept, value, placeholder, onChange, ...rest } = props;
+  const {
+    autoFocus,
+    className,
+    accept,
+    value,
+    placeholder,
+    onChange,
+    ...rest
+  } = props;
 
   assertEmpty(rest);
 
+  const inputRef = useAutoFocus<HTMLButtonElement>(autoFocus);
+  const mergedRef = useMergeRefs([ref, inputRef]);
+
   return (
     <MantineFileInput
       size={"xs"}
       className={className}
-      ref={ref}
+      ref={mergedRef}
       accept={accept}
       value={value}
       placeholder={placeholder}
diff --git a/packages/mantine/src/panel/PanelTextInput.tsx b/packages/mantine/src/panel/PanelTextInput.tsx
index c5ab726f64..744eccdcfc 100644
--- a/packages/mantine/src/panel/PanelTextInput.tsx
+++ b/packages/mantine/src/panel/PanelTextInput.tsx
@@ -1,23 +1,34 @@
 import { TextInput as MantineTextInput } from "@mantine/core";
 
 import { assertEmpty } from "@blocknote/core";
-import { ComponentProps } from "@blocknote/react";
+import { ComponentProps, useAutoFocus, useMergeRefs } from "@blocknote/react";
 import { forwardRef } from "react";
 
 export const PanelTextInput = forwardRef<
   HTMLInputElement,
   ComponentProps["FilePanel"]["TextInput"]
 >((props, ref) => {
-  const { className, value, placeholder, onKeyDown, onChange, ...rest } = props;
+  const {
+    autoFocus,
+    className,
+    value,
+    placeholder,
+    onKeyDown,
+    onChange,
+    ...rest
+  } = props;
 
   assertEmpty(rest);
 
+  const inputRef = useAutoFocus<HTMLInputElement>(autoFocus);
+  const mergedRef = useMergeRefs([ref, inputRef]);
+
   return (
     <MantineTextInput
       size={"xs"}
       data-test={"embed-input"}
       className={className}
-      ref={ref}
+      ref={mergedRef}
       value={value}
       placeholder={placeholder}
       onKeyDown={onKeyDown}
diff --git a/packages/react/src/components/FilePanel/DefaultTabs/EmbedTab.tsx b/packages/react/src/components/FilePanel/DefaultTabs/EmbedTab.tsx
index 52ef673e3b..f9bec2c9bd 100644
--- a/packages/react/src/components/FilePanel/DefaultTabs/EmbedTab.tsx
+++ b/packages/react/src/components/FilePanel/DefaultTabs/EmbedTab.tsx
@@ -75,6 +75,7 @@ export const EmbedTab = <
         }
       >
         <Components.FilePanel.TextInput
+          autoFocus
           className={"bn-text-input"}
           placeholder={dict.file_panel.embed.url_placeholder}
           value={currentURL}
diff --git a/packages/react/src/components/FilePanel/DefaultTabs/UploadTab.tsx b/packages/react/src/components/FilePanel/DefaultTabs/UploadTab.tsx
index a3b0be2138..240d23d593 100644
--- a/packages/react/src/components/FilePanel/DefaultTabs/UploadTab.tsx
+++ b/packages/react/src/components/FilePanel/DefaultTabs/UploadTab.tsx
@@ -91,6 +91,7 @@ export const UploadTab = <
   return (
     <Components.FilePanel.TabPanel className={"bn-tab-panel"}>
       <Components.FilePanel.FileInput
+        autoFocus
         className="bn-file-input"
         data-test="upload-input"
         accept={accept}
diff --git a/packages/react/src/components/FilePanel/FilePanelController.tsx b/packages/react/src/components/FilePanel/FilePanelController.tsx
index 682dc95f00..9ece7899ca 100644
--- a/packages/react/src/components/FilePanel/FilePanelController.tsx
+++ b/packages/react/src/components/FilePanel/FilePanelController.tsx
@@ -45,7 +45,12 @@ export const FilePanelController = (props: {
         ...props.floatingUIOptions?.useFloatingOptions,
       },
       focusManagerProps: {
-        disabled: true,
+        // Move keyboard focus into the panel when it opens, including when
+        // inserting a file block from the slash menu.
+        disabled: false,
+        // The default panel focuses its input. Custom panels retain the
+        // focus manager's default of focusing their first control.
+        initialFocus: props.filePanel ? 0 : -1,
         ...props.floatingUIOptions?.focusManagerProps,
       },
       elementProps: {
@@ -55,7 +60,7 @@ export const FilePanelController = (props: {
         ...props.floatingUIOptions?.elementProps,
       },
     }),
-    [blockId, editor, filePanel, props.floatingUIOptions],
+    [blockId, editor, filePanel, props.filePanel, props.floatingUIOptions],
   );
 
   const Component = props.filePanel || FilePanel;
diff --git a/packages/react/src/components/FilePanel/a11y/FilePanel.a11y.test.ts b/packages/react/src/components/FilePanel/a11y/FilePanel.a11y.test.ts
new file mode 100644
index 0000000000..d2623fcf4f
--- /dev/null
+++ b/packages/react/src/components/FilePanel/a11y/FilePanel.a11y.test.ts
@@ -0,0 +1,34 @@
+import { expect, test } from "vite-plus/test";
+import { page, userEvent } from "vite-plus/test/browser";
+import { openEditor, pressKey } from "@root/tests/a11y/helpers.js";
+
+async function openImagePanel() {
+  await pressKey("Tab");
+  await expect.element(page.getByRole("textbox")).toHaveFocus();
+  await userEvent.keyboard("/image");
+  await expect
+    .element(page.getByRole("option", { name: /Image/ }))
+    .toBeVisible();
+  await pressKey("Enter");
+  const panel = page.elementLocator(
+    document.querySelector<HTMLElement>(".bn-panel")!,
+  );
+  await expect.element(panel).toBeVisible();
+  return panel;
+}
+
+test("file panel: Embed URL input receives focus on opening", async () => {
+  await openEditor([{ type: "paragraph" }]);
+  const panel = await openImagePanel();
+  await expect.element(panel.getByPlaceholder("Enter URL")).toHaveFocus();
+});
+
+test("file panel: Upload button receives focus on opening", async () => {
+  await openEditor([{ type: "paragraph" }], {
+    uploadFile: async () => "/image.svg",
+  });
+  const panel = await openImagePanel();
+  await expect
+    .element(panel.getByRole("button", { name: "Upload image", exact: true }))
+    .toHaveFocus();
+});
diff --git a/packages/react/src/editor/ComponentsContext.tsx b/packages/react/src/editor/ComponentsContext.tsx
index 12bd1791ca..95fd15a575 100644
--- a/packages/react/src/editor/ComponentsContext.tsx
+++ b/packages/react/src/editor/ComponentsContext.tsx
@@ -115,6 +115,7 @@ export type ComponentProps = {
       | { children?: undefined; label: string }
     );
     FileInput: {
+      autoFocus?: boolean;
       className?: string;
       accept: string;
       value: File | null;
@@ -126,6 +127,7 @@ export type ComponentProps = {
       children?: ReactNode;
     };
     TextInput: {
+      autoFocus?: boolean;
       className?: string;
       value: string;
       placeholder: string;
diff --git a/packages/shadcn/src/panel/PanelFileInput.tsx b/packages/shadcn/src/panel/PanelFileInput.tsx
index 3c4f2cbc75..120a0502a0 100644
--- a/packages/shadcn/src/panel/PanelFileInput.tsx
+++ b/packages/shadcn/src/panel/PanelFileInput.tsx
@@ -1,5 +1,5 @@
 import { assertEmpty } from "@blocknote/core";
-import { ComponentProps } from "@blocknote/react";
+import { ComponentProps, useAutoFocus, useMergeRefs } from "@blocknote/react";
 import { forwardRef } from "react";
 
 import { useShadCNComponentsContext } from "../ShadCNComponentsContext.js";
@@ -8,17 +8,28 @@ export const PanelFileInput = forwardRef<
   HTMLInputElement,
   ComponentProps["FilePanel"]["FileInput"]
 >((props, ref) => {
-  const { className, accept, value, placeholder, onChange, ...rest } = props;
+  const {
+    autoFocus,
+    className,
+    accept,
+    value,
+    placeholder,
+    onChange,
+    ...rest
+  } = props;
 
   assertEmpty(rest);
 
+  const inputRef = useAutoFocus<HTMLInputElement>(autoFocus);
+  const mergedRef = useMergeRefs([ref, inputRef]);
+
   const ShadCNComponents = useShadCNComponentsContext()!;
 
   return (
     <ShadCNComponents.Input.Input
       type={"file"}
       className={className}
-      ref={ref}
+      ref={mergedRef}
       accept={accept}
       value={value ? value.name : undefined}
       onChange={async (e) => onChange?.(e.target.files![0])}
diff --git a/packages/shadcn/src/panel/PanelTextInput.tsx b/packages/shadcn/src/panel/PanelTextInput.tsx
index 8165271d96..98980dfbea 100644
--- a/packages/shadcn/src/panel/PanelTextInput.tsx
+++ b/packages/shadcn/src/panel/PanelTextInput.tsx
@@ -1,5 +1,5 @@
 import { assertEmpty } from "@blocknote/core";
-import { ComponentProps } from "@blocknote/react";
+import { ComponentProps, useAutoFocus, useMergeRefs } from "@blocknote/react";
 import { forwardRef } from "react";
 
 import { cn } from "../lib/utils.js";
@@ -9,17 +9,28 @@ export const PanelTextInput = forwardRef<
   HTMLInputElement,
   ComponentProps["FilePanel"]["TextInput"]
 >((props, ref) => {
-  const { className, value, placeholder, onKeyDown, onChange, ...rest } = props;
+  const {
+    autoFocus,
+    className,
+    value,
+    placeholder,
+    onKeyDown,
+    onChange,
+    ...rest
+  } = props;
 
   assertEmpty(rest);
 
+  const inputRef = useAutoFocus<HTMLInputElement>(autoFocus);
+  const mergedRef = useMergeRefs([ref, inputRef]);
+
   const ShadCNComponents = useShadCNComponentsContext()!;
 
   return (
     <ShadCNComponents.Input.Input
       data-test={"embed-input"}
       className={cn(className, "w-80 max-w-full")}
-      ref={ref}
+      ref={mergedRef}
       value={value}
       placeholder={placeholder}
       onKeyDown={onKeyDown}
diff --git a/tests/a11y/helpers.tsx b/tests/a11y/helpers.tsx
index 18ec817990..19eb5cc2e6 100644
--- a/tests/a11y/helpers.tsx
+++ b/tests/a11y/helpers.tsx
@@ -1,4 +1,4 @@
-import type { PartialBlock } from "@blocknote/core";
+import type { BlockNoteEditor, PartialBlock } from "@blocknote/core";
 import "@blocknote/core/fonts/inter.css";
 import { BlockNoteView } from "@blocknote/mantine";
 import "@blocknote/mantine/style.css";
@@ -27,12 +27,14 @@ function EditorFixture({
   initialContent,
   editable,
   theme,
+  uploadFile,
 }: {
   initialContent: PartialBlock[];
   editable: boolean;
   theme: "light" | "dark";
+  uploadFile?: BlockNoteEditor["uploadFile"];
 }) {
-  const editor = useCreateBlockNote({ initialContent });
+  const editor = useCreateBlockNote({ initialContent, uploadFile });
   return (
     <main style={{ maxWidth: 900, margin: "80px auto", padding: 24 }}>
       <h1>BlockNote accessibility fixture</h1>
@@ -48,7 +50,12 @@ export async function openEditor(
   {
     editable = true,
     theme = "light",
-  }: { editable?: boolean; theme?: "light" | "dark" } = {},
+    uploadFile,
+  }: {
+    editable?: boolean;
+    theme?: "light" | "dark";
+    uploadFile?: BlockNoteEditor["uploadFile"];
+  } = {},
 ) {
   await page.viewport(1280, 900);
   await render(
@@ -56,6 +63,7 @@ export async function openEditor(
       initialContent={initialContent}
       editable={editable}
       theme={theme}
+      uploadFile={uploadFile}
     />,
   );
   await expect.element(page.getByRole("textbox")).toBeVisible();