diff --git a/app/assets/javascripts/filtered_search/filtered_search_dropdown_manager.js.es6 b/app/assets/javascripts/filtered_search/filtered_search_dropdown_manager.js.es6
index 547989a6ff5..8ce4cf4fc36 100644
--- a/app/assets/javascripts/filtered_search/filtered_search_dropdown_manager.js.es6
+++ b/app/assets/javascripts/filtered_search/filtered_search_dropdown_manager.js.es6
@@ -2,7 +2,8 @@
 
 (() => {
   class FilteredSearchDropdownManager {
-    constructor() {
+    constructor(baseEndpoint = '') {
+      this.baseEndpoint = baseEndpoint.replace(/\/$/, '');
       this.tokenizer = gl.FilteredSearchTokenizer;
       this.filteredSearchInput = document.querySelector('.filtered-search');
 
@@ -38,13 +39,13 @@
         milestone: {
           reference: null,
           gl: 'DropdownNonUser',
-          extraArguments: ['milestones.json', '%'],
+          extraArguments: [`${this.baseEndpoint}/milestones.json`, '%'],
           element: document.querySelector('#js-dropdown-milestone'),
         },
         label: {
           reference: null,
           gl: 'DropdownNonUser',
-          extraArguments: ['labels.json', '~'],
+          extraArguments: [`${this.baseEndpoint}/labels.json`, '~'],
           element: document.querySelector('#js-dropdown-label'),
         },
         hint: {
diff --git a/app/assets/javascripts/filtered_search/filtered_search_manager.js.es6 b/app/assets/javascripts/filtered_search/filtered_search_manager.js.es6
index 4e02ab7c8c1..ffc7d29e4c5 100644
--- a/app/assets/javascripts/filtered_search/filtered_search_manager.js.es6
+++ b/app/assets/javascripts/filtered_search/filtered_search_manager.js.es6
@@ -6,7 +6,7 @@
 
       if (this.filteredSearchInput) {
         this.tokenizer = gl.FilteredSearchTokenizer;
-        this.dropdownManager = new gl.FilteredSearchDropdownManager();
+        this.dropdownManager = new gl.FilteredSearchDropdownManager(this.filteredSearchInput.getAttribute('data-base-endpoint') || '');
 
         this.bindEvents();
         this.loadSearchParamsFromURL();
diff --git a/app/views/shared/issuable/_search_bar.html.haml b/app/views/shared/issuable/_search_bar.html.haml
index 173fa922f56..6e417aa2251 100644
--- a/app/views/shared/issuable/_search_bar.html.haml
+++ b/app/views/shared/issuable/_search_bar.html.haml
@@ -11,7 +11,7 @@
             class: "check_all_issues left"
       .issues-other-filters.filtered-search-container
         .filtered-search-input-container
-          %input.form-control.filtered-search{ placeholder: 'Search or filter results...', 'data-id' => 'filtered-search', 'data-project-id' => @project.id, 'data-username-params' => @users.to_json(only: [:id, :username]) }
+          %input.form-control.filtered-search{ placeholder: 'Search or filter results...', 'data-id' => 'filtered-search', 'data-project-id' => @project.id, 'data-username-params' => @users.to_json(only: [:id, :username]), 'data-base-endpoint' => namespace_project_path(@project.namespace, @project) }
           = icon('filter')
           %button.clear-search.hidden{ type: 'button' }
             = icon('times')
diff --git a/spec/features/issues/filtered_search/filter_issues_spec.rb b/spec/features/issues/filtered_search/filter_issues_spec.rb
index 3f70a6aa75f..6f7046c8461 100644
--- a/spec/features/issues/filtered_search/filter_issues_spec.rb
+++ b/spec/features/issues/filtered_search/filter_issues_spec.rb
@@ -801,4 +801,26 @@ describe 'Filter issues', js: true, feature: true do
       expect(auto_discovery_params).to include('assignee_id' => [user.id.to_s])
     end
   end
+
+  context 'URL has a trailing slash' do
+    before do
+      visit "#{namespace_project_issues_path(project.namespace, project)}/"
+    end
+
+    it 'milestone dropdown loads milestones' do
+      input_filtered_search("milestone:", submit: false)
+
+      within('#js-dropdown-milestone') do
+        expect(page).to have_selector('.filter-dropdown .filter-dropdown-item', count: 2)
+      end
+    end
+
+    it 'label dropdown load labels' do
+      input_filtered_search("label:", submit: false)
+
+      within('#js-dropdown-label') do
+        expect(page).to have_selector('.filter-dropdown .filter-dropdown-item', count: 5)
+      end
+    end
+  end
 end