diff --git a/components/email/__tests__/composer-template-reply.test.tsx b/components/email/__tests__/composer-template-reply.test.tsx
new file mode 100644
index 000000000..f804dde67
--- /dev/null
+++ b/components/email/__tests__/composer-template-reply.test.tsx
@@ -0,0 +1,275 @@
+import { act, fireEvent, render, screen, waitFor } from '@testing-library/react';
+import { afterAll, afterEach, beforeAll, describe, expect, it, vi } from 'vitest';
+import React from 'react';
+import type { Editor } from '@tiptap/core';
+import { EmailComposer } from '../email-composer';
+import { useSettingsStore } from '@/stores/settings-store';
+
+// The real composer around the real editor: applying a template to a reply
+// the user has already started (#911, follow-up to #540).
+
+const TEMPLATE = vi.hoisted(() => ({
+  id: 'tpl-1',
+  name: 'Greeting',
+  category: '',
+  subject: '',
+  body: 'Dear reader',
+  isHTML: false,
+  isFavorite: false,
+  createdAt: '2026-01-01T00:00:00.000Z',
+  updatedAt: '2026-01-01T00:00:00.000Z',
+}));
+
+vi.mock('@/components/ui/avatar', () => ({ Avatar: () => null }));
+vi.mock('@/components/plugins/plugin-slot', () => ({ PluginSlot: () => null }));
+vi.mock('@/components/identity/sub-address-helper', () => ({ SubAddressHelper: () => null }));
+// The picker hands the composer a template, as choosing one does. It takes
+// the focus away from the editor first, as the real dialog does.
+vi.mock('@/components/templates/template-picker', () => ({
+  TemplatePicker: ({ onSelect }: { onSelect: (t: unknown, v: Record<string, string>) => void }) =>
+    React.createElement('button', { 'data-testid': 'pick-template', onClick: () => onSelect(TEMPLATE, {}) }, 'pick'),
+}));
+vi.mock('@/components/templates/template-form', () => ({ TemplateForm: () => null }));
+vi.mock('@/components/files/file-preview-modal', () => ({ FilePreviewModal: () => null }));
+vi.mock('@/hooks/use-focus-trap', () => ({
+  useFocusTrap: () => ({ current: null }),
+}));
+vi.mock('@/hooks/use-pro-multi-account-identities', () => ({
+  useProMultiAccountIdentities: () => ({ enabled: false, groups: [], allIdentities: [] }),
+  stripCrossAccountIdentityPrefix: (id: string) => ({ localAccountId: null, rawId: id }),
+}));
+
+// ─── Store mocks ──────────────────────────────────────────────────────────────
+
+vi.mock('@/stores/auth-store', () => {
+  const state = {
+    client: null,
+    identities: [],
+    primaryIdentity: null,
+    isAuthenticated: false,
+    isDemoMode: false,
+    activeAccountId: null,
+    connectionLost: false,
+    getClientForAccount: () => undefined,
+    getAllConnectedClients: () => new Map(),
+    syncIdentities: () => {},
+    refreshIdentities: async () => {},
+  };
+  const hook = (sel?: (s: typeof state) => unknown) =>
+    typeof sel === 'function' ? sel(state) : state;
+  hook.getState = () => state;
+  hook.setState = (p: Partial<typeof state>) => Object.assign(state, p);
+  return { useAuthStore: hook };
+});
+
+vi.mock('@/stores/identity-store', () => {
+  const state = {
+    identities: [{ id: 'id-me', email: 'me@example.com', name: 'Me', htmlSignature: '<p>Cheers, Me</p>' }],
+    defaultIdentityId: 'id-me',
+  };
+  const hook = (sel?: (s: typeof state) => unknown) =>
+    typeof sel === 'function' ? sel(state) : state;
+  hook.getState = () => state;
+  hook.setState = (p: Partial<typeof state>) => Object.assign(state, p);
+  return { useIdentityStore: hook };
+});
+
+vi.mock('@/stores/account-store', () => {
+  const state = { accounts: [], getAccountById: () => undefined };
+  const hook = (sel?: (s: typeof state) => unknown) =>
+    typeof sel === 'function' ? sel(state) : state;
+  hook.getState = () => state;
+  hook.setState = (p: Partial<typeof state>) => Object.assign(state, p);
+  return { useAccountStore: hook };
+});
+
+vi.mock('@/stores/email-store', () => {
+  const state = {
+    draftSaveEnabled: false,
+    sendRawEmail: async () => ({ sent: true }),
+  };
+  const hook = (sel?: (s: typeof state) => unknown) =>
+    typeof sel === 'function' ? sel(state) : state;
+  hook.getState = () => state;
+  hook.setState = (p: Partial<typeof state>) => Object.assign(state, p);
+  return { useEmailStore: hook };
+});
+
+vi.mock('@/stores/settings-store', () => {
+  const state = {
+    timeFormat: '24h',
+    plainTextMode: false,
+    subAddressDelimiter: '+',
+    autoSelectReplyIdentity: true,
+    attachmentReminderEnabled: false,
+    attachmentReminderKeywords: [],
+    emptySubjectWarningEnabled: true,
+    recipientMentionsEnabled: false,
+    sendDelaySeconds: 0,
+    signaturePosition: 'above_quote',
+    signatureSeparatorEnabled: false,
+    requestReadReceiptDefault: false,
+    externalContentPolicy: 'block',
+    isSenderTrusted: () => false,
+    addTrustedSender: () => {},
+    trustedSendersAddressBook: null,
+    updateSetting: () => {},
+  };
+  const hook = (sel?: (s: typeof state) => unknown) =>
+    typeof sel === 'function' ? sel(state) : state;
+  hook.getState = () => state;
+  hook.setState = (p: Partial<typeof state>) => Object.assign(state, p);
+  return { useSettingsStore: hook, registerTemplateSyncBridge: () => {} };
+});
+
+vi.mock('@/stores/contact-store', () => {
+  const state = {
+    contacts: [],
+    getAutocomplete: async () => [],
+    addToTrustedSendersBook: async () => {},
+  };
+  const hook = (sel?: (s: typeof state) => unknown) =>
+    typeof sel === 'function' ? sel(state) : state;
+  hook.getState = () => state;
+  hook.setState = (p: Partial<typeof state>) => Object.assign(state, p);
+  return { useContactStore: hook };
+});
+
+// ─── Misc dependency mocks ────────────────────────────────────────────────────
+
+vi.mock('@/stores/toast-store', () => ({
+  toast: { info: () => {}, error: () => {}, success: () => {} },
+}));
+
+vi.mock('@/lib/plugin-hooks', () => ({
+  identityHooks: {
+    onSignatureRender: { size: 0, transform: async (value: unknown) => value },
+    onIdentitySelect: { size: 0, emit: async () => {} },
+  },
+  templateHooks: {
+    onTemplateRender: { size: 0, transform: async (value: unknown) => value },
+    onTemplateApply: { size: 0, emit: async () => {} },
+  },
+  emailHooks: {
+    onComposerOpen: { call: async () => [] },
+    onRecipientChange: { call: async () => [] },
+    getRecipientSuggestions: { call: async () => [] },
+    onRecipientChipsChange: { transform: async (chips: unknown) => chips },
+    onDraftChange: { emit: () => {} },
+    onBeforeDraftAutoSave: { transform: async (draft: unknown) => draft },
+    onBeforeEmailSend: { intercept: async () => true, interceptOutcome: async () => 'allowed' },
+    onComposeSend: { takeOver: async () => 'default' },
+    onTransformOutgoingEmail: { transform: async (email: unknown) => email },
+  },
+  contactHooks: {
+    search: { call: async () => [] },
+    onProvideRecipientSuggestions: { transform: async (initial: unknown) => initial },
+  },
+}));
+
+vi.mock('@/lib/email-threading', () => ({
+  computeReplyThreadingHeaders: () => ({ inReplyTo: [], references: [] }),
+}));
+vi.mock('@/lib/debug', () => ({ debug: { log: () => {}, warn: () => {}, error: () => {} } }));
+
+// ─── Tests ────────────────────────────────────────────────────────────────────
+
+const REPLY_TO = {
+  from: [{ email: 'bob@example.com', name: 'Bob' }],
+  to: [{ email: 'me@example.com', name: 'Me' }],
+  subject: 'Lunch',
+  htmlBody: '<p>Original message</p>',
+  receivedAt: '2026-01-01T10:00:00.000Z',
+};
+
+const nextFrame = () => act(() => new Promise<void>((resolve) => requestAnimationFrame(() => resolve())));
+
+async function openReply() {
+  render(<EmailComposer mode="reply" replyTo={REPLY_TO} />);
+  const dom = await waitFor(() => {
+    const el = document.querySelector('.ProseMirror') as (HTMLElement & { editor?: Editor }) | null;
+    expect(el?.editor).toBeTruthy();
+    return el!;
+  });
+  await nextFrame();
+  return dom.editor!;
+}
+
+async function applyTemplate() {
+  act(() => { fireEvent.keyDown(window, { key: 't' }); });
+  const pick = await screen.findByTestId('pick-template');
+  // The picker dialog takes the focus.
+  act(() => { pick.focus(); });
+  fireEvent.click(pick);
+  await waitFor(() => expect(screen.queryByTestId('pick-template')).toBeNull());
+  await nextFrame();
+}
+
+/** Top-level blocks as text, so the order of greeting, template, signature and quote shows. */
+const blocks = (editor: Editor) => {
+  const out: string[] = [];
+  editor.state.doc.forEach((node) => {
+    if (node.type.name === 'quotedHtml') out.push(`[quote:${new DOMParser().parseFromString(node.attrs.html as string, 'text/html').body.textContent}]`);
+    else if (node.type.name === 'signatureBlock') out.push('[signature]');
+    else if (node.textContent) out.push(node.textContent);
+  });
+  return out;
+};
+
+describe('applying a template to a reply (#911)', () => {
+  const range = Range.prototype as unknown as Record<string, unknown>;
+  const doc = document as unknown as Record<string, unknown>;
+  beforeAll(() => {
+    range.getClientRects = () => [];
+    range.getBoundingClientRect = () => ({ x: 0, y: 0, width: 0, height: 0, top: 0, right: 0, bottom: 0, left: 0 });
+    doc.elementFromPoint = () => null;
+  });
+  afterAll(() => {
+    delete range.getClientRects;
+    delete range.getBoundingClientRect;
+    delete doc.elementFromPoint;
+  });
+  afterEach(() => {
+    useSettingsStore.setState({ signaturePosition: 'above_quote', plainTextMode: false });
+  });
+
+  // The user starts typing right away, at the caret the reply opened with.
+  it('keeps the greeting and puts the template after it, above the signature and the quote', async () => {
+    const editor = await openReply();
+    act(() => { editor.view.dispatch(editor.state.tr.insertText('Hello Mr. X')); });
+
+    await applyTemplate();
+
+    expect(blocks(editor)).toEqual(['Hello Mr. X', 'Dear reader', '[signature]', 'reply_line', '[quote:Original message]']);
+  });
+
+  it('does the same when the signature goes below the quote', async () => {
+    useSettingsStore.setState({ signaturePosition: 'below_quote' });
+    const editor = await openReply();
+    act(() => { editor.view.dispatch(editor.state.tr.insertText('Hello Mr. X')); });
+
+    await applyTemplate();
+
+    expect(blocks(editor)).toEqual(['Hello Mr. X', 'Dear reader', 'reply_line', '[quote:Original message]']);
+  });
+
+  it('keeps the greeting in a plain text reply', async () => {
+    useSettingsStore.setState({ plainTextMode: true });
+    render(<EmailComposer mode="reply" replyTo={REPLY_TO} />);
+    const textarea = await waitFor(() => {
+      const el = document.querySelector('textarea');
+      expect(el).toBeTruthy();
+      expect(document.activeElement).toBe(el);
+      return el as HTMLTextAreaElement;
+    });
+    const caret = textarea.selectionStart;
+    fireEvent.change(textarea, {
+      target: { value: textarea.value.slice(0, caret) + 'Hello Mr. X' + textarea.value.slice(caret) },
+    });
+    textarea.setSelectionRange(caret + 11, caret + 11);
+
+    await applyTemplate();
+
+    expect(textarea.value).toBe('Hello Mr. XDear reader\n\nCheers, Me\n\nreply_line\n> Original message');
+  });
+});