diff --git a/app/javascript/flavours/glitch/actions/compose.js b/app/javascript/flavours/glitch/actions/compose.js
index 464ba6a0c2..2754309fbe 100644
--- a/app/javascript/flavours/glitch/actions/compose.js
+++ b/app/javascript/flavours/glitch/actions/compose.js
@@ -6,7 +6,6 @@ import { throttle } from 'lodash';
 import api from 'flavours/glitch/api';
 import { browserHistory } from 'flavours/glitch/components/router';
 import { countableText } from 'flavours/glitch/features/compose/util/counter';
-import { search as emojiSearch } from 'flavours/glitch/features/emoji/emoji_mart_search_light';
 import { tagHistory } from 'flavours/glitch/settings';
 import { fetchCustomEmojiData } from '@/flavours/glitch/features/emoji/picker';
 import { recoverHashtags } from 'flavours/glitch/utils/hashtag';
@@ -627,7 +626,8 @@ const fetchComposeSuggestionsAccounts = throttle((dispatch, token) => {
 
 const fetchComposeSuggestionsEmojis = async (dispatch, token) => {
   const custom = await fetchCustomEmojiData();
-  const results = emojiSearch(token.replace(':', ''), { maxResults: 5, custom });
+  const { search } = await import('@/flavours/glitch/features/emoji/emoji_mart_search_light');
+  const results = search(token.replace(':', ''), { maxResults: 5, custom });
   dispatch(readyComposeSuggestionsEmojis(token, results));
 };
 
diff --git a/app/javascript/flavours/glitch/components/autosuggest_emoji.jsx b/app/javascript/flavours/glitch/components/autosuggest_emoji.jsx
deleted file mode 100644
index 892d068b31..0000000000
--- a/app/javascript/flavours/glitch/components/autosuggest_emoji.jsx
+++ /dev/null
@@ -1,43 +0,0 @@
-import PropTypes from 'prop-types';
-import { PureComponent } from 'react';
-
-import { assetHost } from 'flavours/glitch/utils/config';
-
-import { unicodeMapping } from '../features/emoji/emoji_unicode_mapping_light';
-
-export default class AutosuggestEmoji extends PureComponent {
-
-  static propTypes = {
-    emoji: PropTypes.object.isRequired,
-  };
-
-  render () {
-    const { emoji } = this.props;
-    let url;
-
-    if (emoji.custom) {
-      url = emoji.imageUrl;
-    } else {
-      const mapping = unicodeMapping[emoji.native] || unicodeMapping[emoji.native.replace(/\uFE0F$/, '')];
-
-      if (!mapping) {
-        return null;
-      }
-
-      url = `${assetHost}/emoji/${mapping.filename}.svg`;
-    }
-
-    return (
-      <div className='autosuggest-emoji'>
-        <img
-          className='emojione'
-          src={url}
-          alt={emoji.native || emoji.colons}
-        />
-
-        <div className='autosuggest-emoji__name'>{emoji.colons}</div>
-      </div>
-    );
-  }
-
-}
diff --git a/app/javascript/flavours/glitch/components/autosuggest_emoji.tsx b/app/javascript/flavours/glitch/components/autosuggest_emoji.tsx
new file mode 100644
index 0000000000..8ab9ce1de2
--- /dev/null
+++ b/app/javascript/flavours/glitch/components/autosuggest_emoji.tsx
@@ -0,0 +1,22 @@
+import type { FC } from 'react';
+
+import { useCustomEmojis } from '@/flavours/glitch/hooks/useCustomEmojis';
+
+import { Emoji } from './emoji';
+
+interface LegacyEmoji {
+  colons: string;
+  custom?: boolean;
+  native?: string;
+  imageUrl?: string;
+}
+
+export const AutosuggestEmoji: FC<{ emoji: LegacyEmoji }> = ({ emoji }) => {
+  const emojis = useCustomEmojis();
+  return (
+    <div className='autosuggest-emoji'>
+      <Emoji code={emoji.native ?? emoji.colons} customEmoji={emojis} />
+      <div className='autosuggest-emoji__name'>{emoji.colons}</div>
+    </div>
+  );
+};
diff --git a/app/javascript/flavours/glitch/components/autosuggest_input.jsx b/app/javascript/flavours/glitch/components/autosuggest_input.jsx
index 9e342a353a..445ec601cf 100644
--- a/app/javascript/flavours/glitch/components/autosuggest_input.jsx
+++ b/app/javascript/flavours/glitch/components/autosuggest_input.jsx
@@ -9,7 +9,7 @@ import Overlay from 'react-overlays/Overlay';
 
 import AutosuggestAccountContainer from '../features/compose/containers/autosuggest_account_container';
 
-import AutosuggestEmoji from './autosuggest_emoji';
+import { AutosuggestEmoji } from './autosuggest_emoji';
 import { AutosuggestHashtag } from './autosuggest_hashtag';
 
 const textAtCursorMatchesToken = (str, caretPosition, searchTokens) => {
diff --git a/app/javascript/flavours/glitch/components/autosuggest_textarea.jsx b/app/javascript/flavours/glitch/components/autosuggest_textarea.jsx
index fae078da31..9b01d300a3 100644
--- a/app/javascript/flavours/glitch/components/autosuggest_textarea.jsx
+++ b/app/javascript/flavours/glitch/components/autosuggest_textarea.jsx
@@ -10,7 +10,7 @@ import Textarea from 'react-textarea-autosize';
 
 import AutosuggestAccountContainer from '../features/compose/containers/autosuggest_account_container';
 
-import AutosuggestEmoji from './autosuggest_emoji';
+import { AutosuggestEmoji } from './autosuggest_emoji';
 import { AutosuggestHashtag } from './autosuggest_hashtag';
 
 const textAtCursorMatchesToken = (str, caretPosition) => {
diff --git a/app/javascript/flavours/glitch/components/emoji/index.tsx b/app/javascript/flavours/glitch/components/emoji/index.tsx
index b2e5e5fb66..3db6da7ed7 100644
--- a/app/javascript/flavours/glitch/components/emoji/index.tsx
+++ b/app/javascript/flavours/glitch/components/emoji/index.tsx
@@ -19,6 +19,7 @@ import {
   stringToEmojiState,
   tokenizeText,
 } from '@/flavours/glitch/features/emoji/render';
+import type { ExtraCustomEmojiMap } from '@/flavours/glitch/features/emoji/types';
 
 import { AnimateEmojiContext, CustomEmojiContext } from './context';
 
@@ -26,14 +27,19 @@ interface EmojiProps {
   code: string;
   showFallback?: boolean;
   showLoading?: boolean;
+  customEmoji?: ExtraCustomEmojiMap | null;
 }
 
 export const Emoji: FC<EmojiProps> = ({
   code,
   showFallback = true,
   showLoading = true,
+  customEmoji: customEmojiOverride,
 }) => {
-  const customEmoji = useContext(CustomEmojiContext);
+  let customEmoji = useContext(CustomEmojiContext);
+  if (customEmojiOverride) {
+    customEmoji = customEmojiOverride;
+  }
 
   // First, set the emoji state based on the input code.
   const [state, setState] = useState(() =>
diff --git a/app/javascript/flavours/glitch/entrypoints/public.tsx b/app/javascript/flavours/glitch/entrypoints/public.tsx
index 173c0075d5..33d791c815 100644
--- a/app/javascript/flavours/glitch/entrypoints/public.tsx
+++ b/app/javascript/flavours/glitch/entrypoints/public.tsx
@@ -13,12 +13,16 @@ import axios from 'axios';
 import { on } from 'delegated-events';
 import { throttle } from 'lodash';
 
+import { determineEmojiMode } from '@/flavours/glitch/features/emoji/mode';
+import { updateHtmlWithEmoji } from '@/flavours/glitch/features/emoji/render';
+import loadKeyboardExtensions from '@/flavours/glitch/load_keyboard_extensions';
+import { loadLocale, getLocale } from '@/flavours/glitch/locales';
+import { loadPolyfills } from '@/flavours/glitch/polyfills';
+import ready from '@/flavours/glitch/ready';
+import { assetHost } from '@/flavours/glitch/utils/config';
+import { getNestedProperty } from '@/flavours/glitch/utils/objects';
+import { isDarkMode } from '@/flavours/glitch/utils/theme';
 import { formatTime } from '@/flavours/glitch/utils/time';
-import emojify from 'flavours/glitch/features/emoji/emoji';
-import loadKeyboardExtensions from 'flavours/glitch/load_keyboard_extensions';
-import { loadLocale, getLocale } from 'flavours/glitch/locales';
-import { loadPolyfills } from 'flavours/glitch/polyfills';
-import ready from 'flavours/glitch/ready';
 
 import 'cocoon-js-vanilla';
 
@@ -37,7 +41,7 @@ const messages = defineMessages({
   },
 });
 
-function loaded() {
+async function loaded() {
   const { messages: localeData } = getLocale();
 
   const locale = document.documentElement.lang;
@@ -74,9 +78,30 @@ function loaded() {
     return messageFormat.format(values) as string;
   };
 
-  document.querySelectorAll('.emojify').forEach((content) => {
-    content.innerHTML = emojify(content.innerHTML);
-  });
+  let emojiStyle = 'auto';
+  const initialStateText =
+    document.getElementById('initial-state')?.textContent;
+  if (initialStateText) {
+    const stateEmojiStyle = getNestedProperty(
+      JSON.parse(initialStateText) as unknown,
+      'meta',
+      'emoji_style',
+    );
+    if (typeof stateEmojiStyle === 'string') {
+      emojiStyle = stateEmojiStyle;
+    }
+  }
+  const emojiMode = determineEmojiMode(emojiStyle);
+  const darkTheme = isDarkMode();
+  for (const element of document.querySelectorAll('.emojify')) {
+    await updateHtmlWithEmoji({
+      assetHost,
+      element,
+      locale,
+      mode: emojiMode,
+      darkTheme,
+    });
+  }
 
   document
     .querySelectorAll<HTMLTimeElement>('time.formatted')
diff --git a/app/javascript/flavours/glitch/features/emoji/emoji.js b/app/javascript/flavours/glitch/features/emoji/emoji.js
deleted file mode 100644
index 09b3c89981..0000000000
--- a/app/javascript/flavours/glitch/features/emoji/emoji.js
+++ /dev/null
@@ -1,170 +0,0 @@
-import Trie from 'substring-trie';
-
-import { getIsSystemTheme, isDarkMode } from '@/flavours/glitch/utils/theme';
-import { assetHost } from 'flavours/glitch/utils/config';
-
-import { autoPlayGif } from '../../initial_state';
-
-import { unicodeMapping } from './emoji_unicode_mapping_light';
-
-const trie = new Trie(Object.keys(unicodeMapping));
-
-// Convert to file names from emojis. (For different variation selector emojis)
-const emojiFilenames = (emojis) => {
-  return emojis.map(v => unicodeMapping[v].filename);
-};
-
-// Emoji requiring extra borders depending on theme
-const darkEmoji = emojiFilenames(['🎱', '🐜', '⚫', '🖤', '⬛', '◼️', '◾', '◼️', '✒️', '▪️', '💣', '🎳', '📷', '📸', '♣️', '🕶️', '✴️', '🔌', '💂‍♀️', '📽️', '🍳', '🦍', '💂', '🔪', '🕳️', '🕹️', '🕋', '🖊️', '🖋️', '💂‍♂️', '🎤', '🎓', '🎥', '🎼', '♠️', '🎩', '🦃', '📼', '📹', '🎮', '🐃', '🏴', '🐞', '🕺', '📱', '📲', '🚲', '🪮', '🐦‍⬛']);
-const lightEmoji = emojiFilenames(['👽', '⚾', '🐔', '☁️', '💨', '🕊️', '👀', '🍥', '👻', '🐐', '❕', '❔', '⛸️', '🌩️', '🔊', '🔇', '📃', '🌧️', '🐏', '🍚', '🍙', '🐓', '🐑', '💀', '☠️', '🌨️', '🔉', '🔈', '💬', '💭', '🏐', '🏳️', '⚪', '⬜', '◽', '◻️', '▫️', '🪽', '🪿']);
-
-/**
- * @param {string} filename
- * @param {"light" | "dark" } colorScheme
- * @returns {string}
- */
-const emojiFilename = (filename, colorScheme) => {
-  const borderedEmoji = colorScheme === "light" ? lightEmoji : darkEmoji;
-  return borderedEmoji.includes(filename) ? (filename + '_border') : filename;
-};
-
-const emojifyTextNode = (node, customEmojis) => {
-  const VS15 = 0xFE0E;
-  const VS16 = 0xFE0F;
-
-  let str = node.textContent;
-
-  const fragment = new DocumentFragment();
-  let i = 0;
-
-  for (;;) {
-    let unicode_emoji;
-
-    // Skip to the next potential emoji to replace (either custom emoji or custom emoji :shortcode:
-    if (customEmojis === null) {
-      while (i < str.length && !(unicode_emoji = trie.search(str.slice(i)))) {
-        i += str.codePointAt(i) < 65536 ? 1 : 2;
-      }
-    } else {
-      while (i < str.length && str[i] !== ':' && !(unicode_emoji = trie.search(str.slice(i)))) {
-        i += str.codePointAt(i) < 65536 ? 1 : 2;
-      }
-    }
-
-    // We reached the end of the string, nothing to replace
-    if (i === str.length) {
-      break;
-    }
-
-    let rend, replacement = null;
-    if (str[i] === ':') { // Potentially the start of a custom emoji :shortcode:
-      rend = str.indexOf(':', i + 1) + 1;
-
-      // no matching ending ':', skip
-      if (!rend) {
-        i++;
-        continue;
-      }
-
-      const shortcode = str.slice(i, rend);
-      const custom_emoji = customEmojis[shortcode];
-
-      // not a recognized shortcode, skip
-      if (!custom_emoji) {
-        i++;
-        continue;
-      }
-
-      // now got a replacee as ':shortcode:'
-      // if you want additional emoji handler, add statements below which set replacement and return true.
-      const filename = autoPlayGif ? custom_emoji.url : custom_emoji.static_url;
-      replacement = document.createElement('img');
-      replacement.setAttribute('draggable', 'false');
-      replacement.setAttribute('class', 'emojione custom-emoji');
-      replacement.setAttribute('alt', shortcode);
-      replacement.setAttribute('title', shortcode);
-      replacement.setAttribute('src', filename);
-      replacement.setAttribute('data-original', custom_emoji.url);
-      replacement.setAttribute('data-static', custom_emoji.static_url);
-    } else { // start of an unicode emoji
-      rend = i + unicode_emoji.length;
-
-      // If the matched character was followed by VS15 (for selecting text presentation), skip it.
-      if (str.codePointAt(rend - 1) !== VS16 && str.codePointAt(rend) === VS15) {
-        i = rend + 1;
-        continue;
-      }
-
-      const { filename, shortCode } = unicodeMapping[unicode_emoji];
-      const title = shortCode ? `:${shortCode}:` : '';
-
-      const isSystemTheme = getIsSystemTheme();
-
-      const theme = (isSystemTheme || !isDarkMode()) ? 'light' : 'dark';
-
-      const imageFilename = emojiFilename(filename, theme);
-
-      const img = document.createElement('img');
-      img.setAttribute('draggable', 'false');
-      img.setAttribute('class', 'emojione');
-      img.setAttribute('alt', unicode_emoji);
-      img.setAttribute('title', title);
-      img.setAttribute('src', `${assetHost}/emoji/${imageFilename}.svg`);
-
-      if (isSystemTheme && imageFilename !== emojiFilename(filename, 'dark')) {
-        replacement = document.createElement('picture');
-
-        const source = document.createElement('source');
-        source.setAttribute('media', '(prefers-color-scheme: dark)');
-        source.setAttribute('srcset', `${assetHost}/emoji/${emojiFilename(filename, 'dark')}.svg`);
-        replacement.appendChild(source);
-        replacement.appendChild(img);
-      } else {
-        replacement = img;
-      }
-    }
-
-    // Add the processed-up-to-now string and the emoji replacement
-    fragment.append(document.createTextNode(str.slice(0, i)));
-    fragment.append(replacement);
-    str = str.slice(rend);
-    i = 0;
-  }
-
-  fragment.append(document.createTextNode(str));
-  node.parentElement.replaceChild(fragment, node);
-};
-
-const emojifyNode = (node, customEmojis) => {
-  for (const child of Array.from(node.childNodes)) {
-    switch(child.nodeType) {
-    case Node.TEXT_NODE:
-      emojifyTextNode(child, customEmojis);
-      break;
-    case Node.ELEMENT_NODE:
-      if (!child.classList.contains('invisible'))
-        emojifyNode(child, customEmojis);
-      break;
-    }
-  }
-};
-
-/**
- * Legacy emoji processing function.
- * @param {string} str
- * @param {object} customEmojis
- * @returns {string}
- */
-const emojify = (str, customEmojis = {}) => {
-  const wrapper = document.createElement('div');
-  wrapper.innerHTML = str;
-
-  if (!Object.keys(customEmojis).length)
-    customEmojis = null;
-
-  emojifyNode(wrapper, customEmojis);
-
-  return wrapper.innerHTML;
-};
-
-export default emojify;
diff --git a/app/javascript/flavours/glitch/features/emoji/emoji_unicode_mapping_light.ts b/app/javascript/flavours/glitch/features/emoji/emoji_unicode_mapping_light.ts
deleted file mode 100644
index ecf36e3ea8..0000000000
--- a/app/javascript/flavours/glitch/features/emoji/emoji_unicode_mapping_light.ts
+++ /dev/null
@@ -1,62 +0,0 @@
-// A mapping of unicode strings to an object containing the filename
-// (i.e. the svg filename) and a shortCode intended to be shown
-// as a "title" attribute in an HTML element (aka tooltip).
-
-import emojiCompressed from 'virtual:mastodon-emoji-compressed';
-import type {
-  FilenameData,
-  ShortCodesToEmojiDataKey,
-} from 'virtual:mastodon-emoji-compressed';
-
-import { unicodeToFilename } from './unicode_utils';
-
-type UnicodeMapping = Record<
-  FilenameData[number][0],
-  {
-    shortCode: ShortCodesToEmojiDataKey;
-    filename: FilenameData[number][number];
-  }
->;
-
-const [
-  shortCodesToEmojiData,
-  _skins,
-  _categories,
-  _short_names,
-  emojisWithoutShortCodes,
-] = emojiCompressed;
-
-// decompress
-const unicodeMapping: UnicodeMapping = {};
-
-function processEmojiMapData(
-  emojiMapData: FilenameData[number],
-  shortCode?: ShortCodesToEmojiDataKey,
-) {
-  const [native, _filename] = emojiMapData;
-  // filename name can be derived from unicodeToFilename
-  const filename = emojiMapData[1] ?? unicodeToFilename(native);
-  unicodeMapping[native] = {
-    shortCode,
-    filename,
-  };
-}
-
-Object.keys(shortCodesToEmojiData).forEach(
-  (shortCode: ShortCodesToEmojiDataKey) => {
-    if (shortCode === undefined) return;
-
-    const emojiData = shortCodesToEmojiData[shortCode];
-    if (!emojiData) return;
-    const [filenameData, _searchData] = emojiData;
-    filenameData.forEach((emojiMapData) => {
-      processEmojiMapData(emojiMapData, shortCode);
-    });
-  },
-);
-
-emojisWithoutShortCodes.forEach((emojiMapData) => {
-  processEmojiMapData(emojiMapData);
-});
-
-export { unicodeMapping };
diff --git a/app/javascript/flavours/glitch/features/emoji/mode.ts b/app/javascript/flavours/glitch/features/emoji/mode.ts
index 92e4749993..9cd45621cc 100644
--- a/app/javascript/flavours/glitch/features/emoji/mode.ts
+++ b/app/javascript/flavours/glitch/features/emoji/mode.ts
@@ -34,6 +34,43 @@ export function useEmojiAppState(): EmojiAppState {
   };
 }
 
+export function getEmojiAppState(): EmojiAppState {
+  const currentLocale = toSupportedLocale(document.documentElement.lang);
+
+  let emojiStyle = 'auto';
+  const initialStateText =
+    document.getElementById('initial-state')?.textContent;
+  if (initialStateText) {
+    try {
+      const state = JSON.parse(initialStateText) as unknown;
+      if (
+        state !== null &&
+        typeof state === 'object' &&
+        'meta' in state &&
+        state.meta !== null &&
+        typeof state.meta === 'object' &&
+        'emoji_style' in state.meta &&
+        typeof state.meta.emoji_style === 'string'
+      ) {
+        emojiStyle = state.meta.emoji_style;
+      }
+    } catch (err: unknown) {
+      console.warn(
+        'Failed to parse initial state for emoji, defaulting to auto. Error:',
+        err,
+      );
+    }
+  }
+
+  return {
+    currentLocale,
+    locales: [currentLocale],
+    mode: determineEmojiMode(emojiStyle),
+    darkTheme: isDarkMode(),
+    assetHost,
+  };
+}
+
 type Feature = Uint8ClampedArray;
 
 // See: https://github.com/nolanlawson/emoji-picker-element/blob/master/src/picker/constants.js
diff --git a/app/javascript/flavours/glitch/features/emoji/normalize.ts b/app/javascript/flavours/glitch/features/emoji/normalize.ts
index 0850a4bf8f..2816f6125c 100644
--- a/app/javascript/flavours/glitch/features/emoji/normalize.ts
+++ b/app/javascript/flavours/glitch/features/emoji/normalize.ts
@@ -152,11 +152,11 @@ const CODES_WITH_LIGHT_BORDER = EMOJIS_WITH_LIGHT_BORDER.map(emojiToUnicodeHex);
 
 export function unicodeHexToUrl({
   unicodeHex,
-  darkTheme,
+  darkTheme = true,
   assetHost,
 }: {
   unicodeHex: string;
-  darkTheme: boolean;
+  darkTheme?: boolean;
   assetHost: string;
 }): string {
   const normalizedHex = unicodeToTwemojiHex(unicodeHex);
diff --git a/app/javascript/flavours/glitch/features/emoji/render.test.ts b/app/javascript/flavours/glitch/features/emoji/render.test.ts
index dffebd1f8c..a668f33d29 100644
--- a/app/javascript/flavours/glitch/features/emoji/render.test.ts
+++ b/app/javascript/flavours/glitch/features/emoji/render.test.ts
@@ -1,11 +1,13 @@
 import { customEmojiFactory, unicodeEmojiFactory } from '@/testing/factories';
 
+import { EMOJI_MODE_TWEMOJI } from './constants';
 import * as db from './database';
 import * as loader from './loader';
 import {
   loadEmojiDataToState,
   stringToEmojiState,
   tokenizeText,
+  updateHtmlWithEmoji,
 } from './render';
 import type { EmojiStateCustom, EmojiStateUnicode } from './types';
 
@@ -107,6 +109,74 @@ describe('stringToEmojiState', () => {
   });
 });
 
+describe('updateHtmlWithEmoji', () => {
+  const defaultOptions = {
+    assetHost: '',
+    darkTheme: false,
+    mode: EMOJI_MODE_TWEMOJI,
+    locale: 'en',
+  } as const;
+
+  beforeEach(() => {
+    vi.clearAllMocks();
+  });
+
+  test('updates element text with emojis', async () => {
+    const element = document.createElement('div');
+    element.textContent = '😊';
+
+    vi.spyOn(db, 'loadLegacyShortcodesByShortcode').mockResolvedValueOnce(
+      undefined,
+    );
+    vi.spyOn(db, 'loadEmojiByHexcode').mockResolvedValueOnce(
+      unicodeEmojiFactory(),
+    );
+
+    await updateHtmlWithEmoji({
+      ...defaultOptions,
+      element,
+    });
+
+    const img = element.querySelector('img');
+    expect(img).toBeDefined();
+  });
+
+  test('does not update element text when mode is native', async () => {
+    const element = document.createElement('div');
+    element.textContent = '😊';
+
+    const dbShortcodeCall = vi.spyOn(db, 'loadLegacyShortcodesByShortcode');
+    const dbEmojiCall = vi.spyOn(db, 'loadEmojiByHexcode');
+
+    await updateHtmlWithEmoji({
+      ...defaultOptions,
+      mode: 'native',
+      element,
+    });
+
+    expect(dbShortcodeCall).not.toHaveBeenCalled();
+    expect(dbEmojiCall).not.toHaveBeenCalled();
+    expect(element.textContent).toBe('😊');
+  });
+
+  test('does not try to load custom emojis', async () => {
+    const element = document.createElement('div');
+    element.textContent = ':smile:';
+
+    const dbShortcodeCall = vi.spyOn(db, 'loadLegacyShortcodesByShortcode');
+    const dbEmojiCall = vi.spyOn(db, 'loadEmojiByHexcode');
+
+    await updateHtmlWithEmoji({
+      ...defaultOptions,
+      element,
+    });
+
+    expect(dbShortcodeCall).not.toHaveBeenCalled();
+    expect(dbEmojiCall).not.toHaveBeenCalled();
+    expect(element.textContent).toBe(':smile:');
+  });
+});
+
 describe('loadEmojiDataToState', () => {
   beforeEach(() => {
     vi.clearAllMocks();
@@ -137,6 +207,18 @@ describe('loadEmojiDataToState', () => {
     });
   });
 
+  test('converts unicode emoji code to hexcode when loading data', async () => {
+    const dbCall = vi
+      .spyOn(db, 'loadEmojiByHexcode')
+      .mockResolvedValue(unicodeEmojiFactory());
+    const unicodeState = {
+      type: 'unicode',
+      code: '😊',
+    } as const satisfies EmojiStateUnicode;
+    await loadEmojiDataToState(unicodeState, 'en');
+    expect(dbCall).toHaveBeenCalledWith('1F60A', 'en');
+  });
+
   test('returns null for custom emoji without data', async () => {
     const customState = {
       type: 'custom',
diff --git a/app/javascript/flavours/glitch/features/emoji/render.ts b/app/javascript/flavours/glitch/features/emoji/render.ts
index 4b65f3abde..affa8e0f16 100644
--- a/app/javascript/flavours/glitch/features/emoji/render.ts
+++ b/app/javascript/flavours/glitch/features/emoji/render.ts
@@ -4,7 +4,9 @@ import {
   EMOJI_TYPE_UNICODE,
   EMOJI_TYPE_CUSTOM,
 } from './constants';
+import { emojiToInversionClassName, unicodeHexToUrl } from './normalize';
 import type {
+  EmojiAppState,
   EmojiLoadedState,
   EmojiMode,
   EmojiState,
@@ -47,14 +49,14 @@ export function tokenizeText(text: string): TokenizedText {
     if (code.startsWith(':') && code.endsWith(':')) {
       // Custom emoji
       tokens.push({
-        type: EMOJI_TYPE_CUSTOM,
         code,
+        type: EMOJI_TYPE_CUSTOM,
       } satisfies EmojiStateCustom);
     } else {
       // Unicode emoji
       tokens.push({
+        code,
         type: EMOJI_TYPE_UNICODE,
-        code: code,
       } satisfies EmojiStateUnicode);
     }
     lastIndex = match.index + code.length;
@@ -76,8 +78,8 @@ export function stringToEmojiState(
 ): EmojiStateUnicode | Required<EmojiStateCustom> | null {
   if (isUnicodeEmoji(code)) {
     return {
-      type: EMOJI_TYPE_UNICODE,
       code: emojiToUnicodeHex(code),
+      type: EMOJI_TYPE_UNICODE,
     };
   }
 
@@ -95,6 +97,68 @@ export function stringToEmojiState(
   return null;
 }
 
+/**
+ * Takes an element and emojifies all native emoji.
+ */
+export async function updateHtmlWithEmoji({
+  assetHost,
+  darkTheme,
+  element,
+  mode,
+  locale,
+}: {
+  element: Element;
+  locale: string;
+} & Omit<EmojiAppState, 'currentLocale' | 'locales'>) {
+  if (mode === EMOJI_MODE_NATIVE) {
+    return;
+  }
+
+  const tokens = tokenizeText(element.innerHTML);
+  const newChildren: (string | Element)[] = [];
+  for (const token of tokens) {
+    if (typeof token === 'string') {
+      newChildren.push(token);
+      continue;
+    }
+
+    const state = await loadEmojiDataToState(token, locale);
+    // Ignore custom emoji if we encounter them.
+    if (!state || state.type === EMOJI_TYPE_CUSTOM) {
+      newChildren.push(token.code);
+      continue;
+    }
+
+    if (!shouldRenderImage(state, mode)) {
+      newChildren.push(state.data.unicode);
+      continue;
+    }
+
+    const img = document.createElement('img');
+    img.src = unicodeHexToUrl({
+      assetHost,
+      darkTheme,
+      unicodeHex: state.data.hexcode,
+    });
+    img.alt = state.data.unicode;
+    img.title = state.data.label;
+    img.classList.add('emojione');
+
+    const inversionClass = emojiToInversionClassName(state.data.unicode);
+    if (inversionClass) {
+      img.classList.add(inversionClass);
+    }
+
+    newChildren.push(img);
+  }
+
+  element.innerHTML = newChildren.reduce<string>(
+    (prev, curr) =>
+      typeof curr === 'string' ? prev + curr : prev + curr.outerHTML,
+    '',
+  );
+}
+
 /**
  * Loads emoji data into the given state if not already loaded.
  * @param state Emoji state to load data for.
@@ -121,17 +185,19 @@ export async function loadEmojiDataToState(
     LocaleNotLoadedError,
   } = await import('./database');
 
+  const code = isUnicodeEmoji(state.code)
+    ? emojiToUnicodeHex(state.code)
+    : state.code;
+
   // First, try to load the data from IndexedDB.
   try {
-    const legacyCode = await loadLegacyShortcodesByShortcode(state.code);
+    const legacyCode = await loadLegacyShortcodesByShortcode(code);
     // This is duplicative, but that's because TS can't distinguish the state type easily.
-    const data = await loadEmojiByHexcode(
-      legacyCode?.hexcode ?? state.code,
-      locale,
-    );
+    const data = await loadEmojiByHexcode(legacyCode?.hexcode ?? code, locale);
     if (data) {
       return {
         ...state,
+        code,
         type: EMOJI_TYPE_UNICODE,
         data,
         // TODO: Use CLDR shortcodes when the picker supports them.
@@ -140,14 +206,14 @@ export async function loadEmojiDataToState(
     }
 
     // If not found, assume it's not an emoji and return null.
-    log('Could not find emoji %s for locale %s', state.code, locale);
+    log('Could not find emoji %s for locale %s', code, locale);
     return null;
   } catch (err: unknown) {
     // If the locale is not loaded, load it and retry once.
     if (!retry && err instanceof LocaleNotLoadedError) {
       log(
         'Error loading emoji %s for locale %s, loading locale and retrying.',
-        state.code,
+        code,
         locale,
       );
       const { importEmojiData } = await import('./loader');
diff --git a/app/javascript/flavours/glitch/utils/objects.test.ts b/app/javascript/flavours/glitch/utils/objects.test.ts
new file mode 100644
index 0000000000..5c08cd0561
--- /dev/null
+++ b/app/javascript/flavours/glitch/utils/objects.test.ts
@@ -0,0 +1,27 @@
+/* eslint-disable @typescript-eslint/no-confusing-void-expression */
+import { getNestedProperty } from './objects';
+
+describe('getNestedProperty', () => {
+  test('returns the value of a nested property if it exists', () => {
+    const obj = { a: { b: { c: 42 } } };
+    expect(getNestedProperty(obj, 'a', 'b', 'c')).toBe(42);
+  });
+
+  test('returns undefined if any part of the path does not exist', () => {
+    const obj = { a: { b: { c: 42 } } };
+    expect(getNestedProperty(obj, 'a', 'x', 'c')).toBeUndefined();
+    expect(getNestedProperty(obj, 'a', 'b', 'x')).toBeUndefined();
+    expect(getNestedProperty(obj, 'x', 'b', 'c')).toBeUndefined();
+  });
+
+  test('returns undefined if the initial object is not a record', () => {
+    expect(getNestedProperty(null, 'a', 'b')).toBeUndefined();
+    expect(getNestedProperty(42, 'a', 'b')).toBeUndefined();
+    expect(getNestedProperty('string', 'a', 'b')).toBeUndefined();
+  });
+
+  test('returns undefined if no keys are provided', () => {
+    const obj = { a: 1 };
+    expect(getNestedProperty(obj)).toBeUndefined();
+  });
+});
diff --git a/app/javascript/flavours/glitch/utils/objects.ts b/app/javascript/flavours/glitch/utils/objects.ts
new file mode 100644
index 0000000000..4430849c0c
--- /dev/null
+++ b/app/javascript/flavours/glitch/utils/objects.ts
@@ -0,0 +1,52 @@
+import { isPlainObject } from '@reduxjs/toolkit';
+
+export type RecordObject = Record<PropertyKey, unknown>;
+
+export function isRecordObject(obj: unknown): obj is RecordObject {
+  return isPlainObject(obj);
+}
+
+type NestedProperty<T, K extends readonly PropertyKey[]> = K extends readonly [
+  infer Head,
+  ...infer Tail,
+]
+  ? Head extends keyof NonNullable<T>
+    ? Tail extends readonly PropertyKey[]
+      ? NestedProperty<NonNullable<T>[Head], Tail>
+      : NonNullable<T>[Head]
+    : undefined
+  : T;
+
+export function getNestedProperty<
+  TObject extends RecordObject,
+  const TKeys extends readonly PropertyKey[],
+>(object: TObject, ...keys: TKeys): NestedProperty<TObject, TKeys> | undefined;
+export function getNestedProperty(
+  object: unknown,
+  ...keys: PropertyKey[]
+): unknown;
+export function getNestedProperty(
+  object: unknown,
+  ...keys: PropertyKey[]
+): unknown {
+  if (!isRecordObject(object) || keys.length === 0) {
+    return undefined;
+  }
+
+  const remainingKeys = [...keys];
+  let currentObject: RecordObject = object;
+  while (remainingKeys.length > 0) {
+    const currentKey = remainingKeys.shift();
+    if (currentKey !== undefined && currentKey in currentObject) {
+      const nextObject = currentObject[currentKey];
+      if (isRecordObject(nextObject)) {
+        currentObject = nextObject;
+        continue;
+      } else if (remainingKeys.length === 0) {
+        return nextObject;
+      }
+    }
+  }
+
+  return undefined;
+}