diff --git a/CHANGELOG.md b/CHANGELOG.md
index 123e5347bb..475edc61c1 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -14,6 +14,7 @@ The format is based on [Keep a Changelog](https://keepachangelog.com/en/1.0.0/).
 - Errors when fetching are now shown with popup errors instead of "Error fetching updates" in panel headers
 - Fixed custom emoji not working in profile field names
 - Fixed pinned statuses not appearing in user profiles
+- Fixed username autocomplete being jumpy
 
 
 ## [2.2.1] - 2020-11-11
diff --git a/src/components/emoji_input/emoji_input.js b/src/components/emoji_input/emoji_input.js
index 87303d0874..2068a598c7 100644
--- a/src/components/emoji_input/emoji_input.js
+++ b/src/components/emoji_input/emoji_input.js
@@ -114,7 +114,8 @@ const EmojiInput = {
       showPicker: false,
       temporarilyHideSuggestions: false,
       keepOpen: false,
-      disableClickOutside: false
+      disableClickOutside: false,
+      suggestions: []
     }
   },
   components: {
@@ -124,21 +125,6 @@ const EmojiInput = {
     padEmoji () {
       return this.$store.getters.mergedConfig.padEmoji
     },
-    suggestions () {
-      const firstchar = this.textAtCaret.charAt(0)
-      if (this.textAtCaret === firstchar) { return [] }
-      const matchedSuggestions = this.suggest(this.textAtCaret)
-      if (matchedSuggestions.length <= 0) {
-        return []
-      }
-      return take(matchedSuggestions, 5)
-        .map(({ imageUrl, ...rest }, index) => ({
-          ...rest,
-          // eslint-disable-next-line camelcase
-          img: imageUrl || '',
-          highlighted: index === this.highlighted
-        }))
-    },
     showSuggestions () {
       return this.focused &&
         this.suggestions &&
@@ -188,6 +174,23 @@ const EmojiInput = {
   watch: {
     showSuggestions: function (newValue) {
       this.$emit('shown', newValue)
+    },
+    textAtCaret: async function (newWord) {
+      const firstchar = newWord.charAt(0)
+      this.suggestions = []
+      if (newWord === firstchar) return
+      const matchedSuggestions = await this.suggest(newWord)
+      // Async: cancel if textAtCaret has changed during wait
+      if (this.textAtCaret !== newWord) return
+      if (matchedSuggestions.length <= 0) return
+      this.suggestions = take(matchedSuggestions, 5)
+        .map(({ imageUrl, ...rest }) => ({
+          ...rest,
+          img: imageUrl || ''
+        }))
+    },
+    suggestions (newValue) {
+      this.$nextTick(this.resize)
     }
   },
   methods: {
diff --git a/src/components/emoji_input/emoji_input.vue b/src/components/emoji_input/emoji_input.vue
index 224e72cf68..107e16c166 100644
--- a/src/components/emoji_input/emoji_input.vue
+++ b/src/components/emoji_input/emoji_input.vue
@@ -37,7 +37,7 @@
           v-for="(suggestion, index) in suggestions"
           :key="index"
           class="autocomplete-item"
-          :class="{ highlighted: suggestion.highlighted }"
+          :class="{ highlighted: index === highlighted }"
           @click.stop.prevent="onClick($event, suggestion)"
         >
           <span class="image">
diff --git a/src/components/emoji_input/suggestor.js b/src/components/emoji_input/suggestor.js
index 8330345bb0..14a2b41edf 100644
--- a/src/components/emoji_input/suggestor.js
+++ b/src/components/emoji_input/suggestor.js
@@ -1,4 +1,3 @@
-import { debounce } from 'lodash'
 /**
  * suggest - generates a suggestor function to be used by emoji-input
  * data: object providing source information for specific types of suggestions:
@@ -11,19 +10,19 @@ import { debounce } from 'lodash'
  * doesn't support user linking you can just provide only emoji.
  */
 
-const debounceUserSearch = debounce((data, input) => {
-  data.updateUsersList(input)
-}, 500)
-
-export default data => input => {
-  const firstChar = input[0]
-  if (firstChar === ':' && data.emoji) {
-    return suggestEmoji(data.emoji)(input)
+export default data => {
+  const emojiCurry = suggestEmoji(data.emoji)
+  const usersCurry = data.store && suggestUsers(data.store)
+  return input => {
+    const firstChar = input[0]
+    if (firstChar === ':' && data.emoji) {
+      return emojiCurry(input)
+    }
+    if (firstChar === '@' && usersCurry) {
+      return usersCurry(input)
+    }
+    return []
   }
-  if (firstChar === '@' && data.users) {
-    return suggestUsers(data)(input)
-  }
-  return []
 }
 
 export const suggestEmoji = emojis => input => {
@@ -57,50 +56,75 @@ export const suggestEmoji = emojis => input => {
     })
 }
 
-export const suggestUsers = data => input => {
-  const noPrefix = input.toLowerCase().substr(1)
-  const users = data.users
+export const suggestUsers = ({ dispatch, state }) => {
+  // Keep some persistent values in closure, most importantly for the
+  // custom debounce to work. Lodash debounce does not return a promise.
+  let suggestions = []
+  let previousQuery = ''
+  let timeout = null
+  let cancelUserSearch = null
 
-  const newUsers = users.filter(
-    user =>
-      user.screen_name.toLowerCase().startsWith(noPrefix) ||
-      user.name.toLowerCase().startsWith(noPrefix)
-
-    /* taking only 20 results so that sorting is a bit cheaper, we display
-     * only 5 anyway. could be inaccurate, but we ideally we should query
-     * backend anyway
-     */
-  ).slice(0, 20).sort((a, b) => {
-    let aScore = 0
-    let bScore = 0
-
-    // Matches on screen name (i.e. user@instance) makes a priority
-    aScore += a.screen_name.toLowerCase().startsWith(noPrefix) ? 2 : 0
-    bScore += b.screen_name.toLowerCase().startsWith(noPrefix) ? 2 : 0
-
-    // Matches on name takes second priority
-    aScore += a.name.toLowerCase().startsWith(noPrefix) ? 1 : 0
-    bScore += b.name.toLowerCase().startsWith(noPrefix) ? 1 : 0
-
-    const diff = (bScore - aScore) * 10
-
-    // Then sort alphabetically
-    const nameAlphabetically = a.name > b.name ? 1 : -1
-    const screenNameAlphabetically = a.screen_name > b.screen_name ? 1 : -1
-
-    return diff + nameAlphabetically + screenNameAlphabetically
-    /* eslint-disable camelcase */
-  }).map(({ screen_name, name, profile_image_url_original }) => ({
-    displayText: screen_name,
-    detailText: name,
-    imageUrl: profile_image_url_original,
-    replacement: '@' + screen_name + ' '
-  }))
-
-  // BE search users to get more comprehensive results
-  if (data.updateUsersList) {
-    debounceUserSearch(data, noPrefix)
+  const userSearch = (query) => dispatch('searchUsers', { query })
+  const debounceUserSearch = (query) => {
+    cancelUserSearch && cancelUserSearch()
+    return new Promise((resolve, reject) => {
+      timeout = setTimeout(() => {
+        userSearch(query).then(resolve).catch(reject)
+      }, 300)
+      cancelUserSearch = () => {
+        clearTimeout(timeout)
+        resolve([])
+      }
+    })
+  }
+
+  return async input => {
+    const noPrefix = input.toLowerCase().substr(1)
+    if (previousQuery === noPrefix) return suggestions
+
+    suggestions = []
+    previousQuery = noPrefix
+    // Fetch more and wait, don't fetch if there's the 2nd @ because
+    // the backend user search can't deal with it.
+    // Reference semantics make it so that we get the updated data after
+    // the await.
+    if (!noPrefix.includes('@')) {
+      await debounceUserSearch(noPrefix)
+    }
+
+    const newSuggestions = state.users.users.filter(
+      user =>
+        user.screen_name.toLowerCase().startsWith(noPrefix) ||
+        user.name.toLowerCase().startsWith(noPrefix)
+    ).slice(0, 20).sort((a, b) => {
+      let aScore = 0
+      let bScore = 0
+
+      // Matches on screen name (i.e. user@instance) makes a priority
+      aScore += a.screen_name.toLowerCase().startsWith(noPrefix) ? 2 : 0
+      bScore += b.screen_name.toLowerCase().startsWith(noPrefix) ? 2 : 0
+
+      // Matches on name takes second priority
+      aScore += a.name.toLowerCase().startsWith(noPrefix) ? 1 : 0
+      bScore += b.name.toLowerCase().startsWith(noPrefix) ? 1 : 0
+
+      const diff = (bScore - aScore) * 10
+
+      // Then sort alphabetically
+      const nameAlphabetically = a.name > b.name ? 1 : -1
+      const screenNameAlphabetically = a.screen_name > b.screen_name ? 1 : -1
+
+      return diff + nameAlphabetically + screenNameAlphabetically
+      /* eslint-disable camelcase */
+    }).map(({ screen_name, name, profile_image_url_original }) => ({
+      displayText: screen_name,
+      detailText: name,
+      imageUrl: profile_image_url_original,
+      replacement: '@' + screen_name + ' '
+    }))
+    /* eslint-enable camelcase */
+
+    suggestions = newSuggestions || []
+    return suggestions
   }
-  return newUsers
-  /* eslint-enable camelcase */
 }
diff --git a/src/components/post_status_form/post_status_form.js b/src/components/post_status_form/post_status_form.js
index 3ff4a3c8e2..4148381c83 100644
--- a/src/components/post_status_form/post_status_form.js
+++ b/src/components/post_status_form/post_status_form.js
@@ -159,8 +159,7 @@ const PostStatusForm = {
           ...this.$store.state.instance.emoji,
           ...this.$store.state.instance.customEmoji
         ],
-        users: this.$store.state.users.users,
-        updateUsersList: (query) => this.$store.dispatch('searchUsers', { query })
+        store: this.$store
       })
     },
     emojiSuggestor () {
diff --git a/src/components/settings_modal/tabs/profile_tab.js b/src/components/settings_modal/tabs/profile_tab.js
index a3e4feafcb..a4fed6294f 100644
--- a/src/components/settings_modal/tabs/profile_tab.js
+++ b/src/components/settings_modal/tabs/profile_tab.js
@@ -68,8 +68,7 @@ const ProfileTab = {
           ...this.$store.state.instance.emoji,
           ...this.$store.state.instance.customEmoji
         ],
-        users: this.$store.state.users.users,
-        updateUsersList: (query) => this.$store.dispatch('searchUsers', { query })
+        store: this.$store
       })
     },
     emojiSuggestor () {
@@ -79,10 +78,7 @@ const ProfileTab = {
       ] })
     },
     userSuggestor () {
-      return suggestor({
-        users: this.$store.state.users.users,
-        updateUsersList: (query) => this.$store.dispatch('searchUsers', { query })
-      })
+      return suggestor({ store: this.$store })
     },
     fieldsLimits () {
       return this.$store.state.instance.fieldsLimits