diff --git a/app/assets/javascripts/awards_handler.js b/app/assets/javascripts/awards_handler.js
index ce426741637..424453436a1 100644
--- a/app/assets/javascripts/awards_handler.js
+++ b/app/assets/javascripts/awards_handler.js
@@ -6,6 +6,7 @@ import { glEmojiTag } from './behaviors/gl_emoji';
 import isEmojiNameValid from './behaviors/gl_emoji/is_emoji_name_valid';
 
 const animationEndEventString = 'animationend webkitAnimationEnd MSAnimationEnd oAnimationEnd';
+const transitionEndEventString = 'transitionend webkitTransitionEnd oTransitionEnd MSTransitionEnd';
 const requestAnimationFrame = window.requestAnimationFrame ||
   window.webkitRequestAnimationFrame ||
   window.mozRequestAnimationFrame ||
@@ -103,8 +104,9 @@ function AwardsHandler() {
     const $glEmojiElement = $target.find('gl-emoji');
     const $spriteIconElement = $target.find('.icon');
     const emoji = ($glEmojiElement.length ? $glEmojiElement : $spriteIconElement).data('name');
+
     $target.closest('.js-awards-block').addClass('current');
-    return this.addAward(this.getVotesBlock(), this.getAwardUrl(), emoji);
+    this.addAward(this.getVotesBlock(), this.getAwardUrl(), emoji);
   });
 }
 
@@ -128,12 +130,12 @@ AwardsHandler.prototype.showEmojiMenu = function showEmojiMenu($addBtn) {
     if ($menu.is('.is-visible')) {
       $addBtn.removeClass('is-active');
       $menu.removeClass('is-visible');
-      $('#emoji_search').blur();
+      $('.js-emoji-menu-search').blur();
     } else {
       $addBtn.addClass('is-active');
       this.positionMenu($menu, $addBtn);
       $menu.addClass('is-visible');
-      $('#emoji_search').focus();
+      $('.js-emoji-menu-search').focus();
     }
   } else {
     $addBtn.addClass('is-loading is-active');
@@ -143,7 +145,7 @@ AwardsHandler.prototype.showEmojiMenu = function showEmojiMenu($addBtn) {
       this.positionMenu($createdMenu, $addBtn);
       return setTimeout(() => {
         $createdMenu.addClass('is-visible');
-        $('#emoji_search').focus();
+        $('.js-emoji-menu-search').focus();
       }, 200);
     });
   }
@@ -174,7 +176,7 @@ AwardsHandler.prototype.createEmojiMenu = function createEmojiMenu(callback) {
 
   const emojiMenuMarkup = `
     <div class="emoji-menu">
-      <input type="text" name="emoji_search" id="emoji_search" value="" class="emoji-search search-input form-control" placeholder="Search emoji" />
+      <input type="text" name="emoji-menu-search" value="" class="js-emoji-menu-search emoji-search search-input form-control" placeholder="Search emoji" />
 
       <div class="emoji-menu-content">
         ${frequentlyUsedCatgegory}
@@ -474,24 +476,41 @@ AwardsHandler.prototype.getFrequentlyUsedEmojis = function getFrequentlyUsedEmoj
 };
 
 AwardsHandler.prototype.setupSearch = function setupSearch() {
-  this.registerEventListener('on', $('input.emoji-search'), 'input', (e) => {
+  const $search = $('.js-emoji-menu-search');
+
+  this.registerEventListener('on', $search, 'input', (e) => {
     const term = $(e.target).val().trim();
-    // Clean previous search results
-    $('ul.emoji-menu-search, h5.emoji-search-title').remove();
-    if (term.length > 0) {
-      // Generate a search result block
-      const h5 = $('<h5 class="emoji-search-title"/>').text('Search results');
-      const foundEmojis = this.searchEmojis(term).show();
-      const ul = $('<ul>').addClass('emoji-menu-list emoji-menu-search').append(foundEmojis);
-      $('.emoji-menu-content ul, .emoji-menu-content h5').hide();
-      $('.emoji-menu-content').append(h5).append(ul);
-    } else {
-      $('.emoji-menu-content').children().show();
+    this.searchEmojis(term);
+  });
+
+  const $menu = $('.emoji-menu');
+  this.registerEventListener('on', $menu, transitionEndEventString, (e) => {
+    if (e.target === e.currentTarget) {
+      // Clear the search
+      this.searchEmojis('');
     }
   });
 };
 
 AwardsHandler.prototype.searchEmojis = function searchEmojis(term) {
+  const $search = $('.js-emoji-menu-search');
+  $search.val(term);
+
+  // Clean previous search results
+  $('ul.emoji-menu-search, h5.emoji-search-title').remove();
+  if (term.length > 0) {
+    // Generate a search result block
+    const h5 = $('<h5 class="emoji-search-title"/>').text('Search results');
+    const foundEmojis = this.findMatchingEmojiElements(term).show();
+    const ul = $('<ul>').addClass('emoji-menu-list emoji-menu-search').append(foundEmojis);
+    $('.emoji-menu-content ul, .emoji-menu-content h5').hide();
+    $('.emoji-menu-content').append(h5).append(ul);
+  } else {
+    $('.emoji-menu-content').children().show();
+  }
+};
+
+AwardsHandler.prototype.findMatchingEmojiElements = function findMatchingEmojiElements(term) {
   const safeTerm = term.toLowerCase();
 
   const namesMatchingAlias = [];
diff --git a/changelogs/unreleased/27655-clear-emoji-search-after-selection.yml b/changelogs/unreleased/27655-clear-emoji-search-after-selection.yml
new file mode 100644
index 00000000000..5fd02696323
--- /dev/null
+++ b/changelogs/unreleased/27655-clear-emoji-search-after-selection.yml
@@ -0,0 +1,4 @@
+---
+title: Clear emoji search in awards menu after picking emoji
+merge_request:
+author:
diff --git a/features/steps/project/issues/award_emoji.rb b/features/steps/project/issues/award_emoji.rb
index a4cfc1fb8c8..dfd0bc13305 100644
--- a/features/steps/project/issues/award_emoji.rb
+++ b/features/steps/project/issues/award_emoji.rb
@@ -87,7 +87,7 @@ class Spinach::Features::AwardEmoji < Spinach::FeatureSteps
   end
 
   step 'I search "hand"' do
-    fill_in 'emoji_search', with: 'hand'
+    fill_in 'emoji-menu-search', with: 'hand'
   end
 
   step 'I see search result for "hand"' do
@@ -101,7 +101,7 @@ class Spinach::Features::AwardEmoji < Spinach::FeatureSteps
   end
 
   step 'The search field is focused' do
-    expect(page).to have_selector('#emoji_search')
-    expect(page.evaluate_script('document.activeElement.id')).to eq('emoji_search')
+    expect(page).to have_selector('.js-emoji-menu-search')
+    expect(page.evaluate_script("document.activeElement.classList.contains('js-emoji-menu-search')")).to eq(true)
   end
 end
diff --git a/spec/javascripts/awards_handler_spec.js b/spec/javascripts/awards_handler_spec.js
index ea7753c7a1d..abb6884fd24 100644
--- a/spec/javascripts/awards_handler_spec.js
+++ b/spec/javascripts/awards_handler_spec.js
@@ -63,7 +63,7 @@ import AwardsHandler from '~/awards_handler';
           $emojiMenu = $('.emoji-menu');
           expect($emojiMenu.length).toBe(1);
           expect($emojiMenu.hasClass('is-visible')).toBe(true);
-          expect($emojiMenu.find('#emoji_search').length).toBe(1);
+          expect($emojiMenu.find('.js-emoji-menu-search').length).toBe(1);
           return expect($('.js-awards-block.current').length).toBe(1);
         });
       });
@@ -194,16 +194,35 @@ import AwardsHandler from '~/awards_handler';
         return expect($thumbsUpEmoji.data("original-title")).toBe('sam');
       });
     });
-    describe('search', function() {
-      return it('should filter the emoji', function(done) {
+    describe('::searchEmojis', () => {
+      it('should filter the emoji', function(done) {
         return openAndWaitForEmojiMenu()
           .then(() => {
             expect($('[data-name=angel]').is(':visible')).toBe(true);
             expect($('[data-name=anger]').is(':visible')).toBe(true);
-            $('#emoji_search').val('ali').trigger('input');
+            awardsHandler.searchEmojis('ali');
             expect($('[data-name=angel]').is(':visible')).toBe(false);
             expect($('[data-name=anger]').is(':visible')).toBe(false);
             expect($('[data-name=alien]').is(':visible')).toBe(true);
+            expect($('.js-emoji-menu-search').val()).toBe('ali');
+          })
+          .then(done)
+          .catch((err) => {
+            done.fail(`Failed to open and build emoji menu: ${err.message}`);
+          });
+      });
+      it('should clear the search when searching for nothing', function(done) {
+        return openAndWaitForEmojiMenu()
+          .then(() => {
+            awardsHandler.searchEmojis('ali');
+            expect($('[data-name=angel]').is(':visible')).toBe(false);
+            expect($('[data-name=anger]').is(':visible')).toBe(false);
+            expect($('[data-name=alien]').is(':visible')).toBe(true);
+            awardsHandler.searchEmojis('');
+            expect($('[data-name=angel]').is(':visible')).toBe(true);
+            expect($('[data-name=anger]').is(':visible')).toBe(true);
+            expect($('[data-name=alien]').is(':visible')).toBe(true);
+            expect($('.js-emoji-menu-search').val()).toBe('');
           })
           .then(done)
           .catch((err) => {
@@ -211,6 +230,7 @@ import AwardsHandler from '~/awards_handler';
           });
       });
     });
+
     describe('emoji menu', function() {
       const emojiSelector = '[data-name="sunglasses"]';
       const openEmojiMenuAndAddEmoji = function() {