diff --git a/app/assets/javascripts/boards/issue_board_filters.js b/app/assets/javascripts/boards/issue_board_filters.js
index 27efb3f775c6dc14eff8c393c60c5aaa90398fc5..aa9dc0fc1583fe134a038692f84986f3cf66ad97 100644
--- a/app/assets/javascripts/boards/issue_board_filters.js
+++ b/app/assets/javascripts/boards/issue_board_filters.js
@@ -1,5 +1,7 @@
+import { BoardType } from 'ee_else_ce/boards/constants';
 import groupBoardMembers from '~/boards/graphql/group_board_members.query.graphql';
 import projectBoardMembers from '~/boards/graphql/project_board_members.query.graphql';
+import usersAutocompleteQuery from '~/graphql_shared/queries/users_autocomplete.query.graphql';
 import groupBoardMilestonesQuery from './graphql/group_board_milestones.query.graphql';
 import projectBoardMilestonesQuery from './graphql/project_board_milestones.query.graphql';
 import boardLabels from './graphql/board_labels.query.graphql';
@@ -14,6 +16,17 @@ export default function issueBoardFilters(apollo, fullPath, isGroupBoard) {
   };
 
   const fetchUsers = (usersSearchTerm) => {
+    if (gon.features?.newGraphqlUsersAutocomplete) {
+      const namespace = isGroupBoard ? BoardType.group : BoardType.project;
+
+      return apollo
+        .query({
+          query: usersAutocompleteQuery,
+          variables: { fullPath, search: usersSearchTerm, isProject: !isGroupBoard },
+        })
+        .then(({ data }) => data[namespace]?.autocompleteUsers);
+    }
+
     return apollo
       .query({
         query: boardAssigneesQuery(),
diff --git a/app/controllers/groups/boards_controller.rb b/app/controllers/groups/boards_controller.rb
index 6bb807be1c439d574b20ea43c66317bbdec169c2..cf0b6cd815a449a501bde99d1020384055f3dde9 100644
--- a/app/controllers/groups/boards_controller.rb
+++ b/app/controllers/groups/boards_controller.rb
@@ -8,6 +8,7 @@ class Groups::BoardsController < Groups::ApplicationController
   before_action do
     push_frontend_feature_flag(:board_multi_select, group)
     push_frontend_feature_flag(:apollo_boards, group)
+    push_frontend_feature_flag(:new_graphql_users_autocomplete, group)
     experiment(:prominent_create_board_btn, subject: current_user) do |e|
       e.control {}
       e.candidate {}
diff --git a/app/controllers/projects/boards_controller.rb b/app/controllers/projects/boards_controller.rb
index 84872d1e97875ea917f6a3ab9443c4babbbe1a38..1c3463fb70c0729abfb2612baf1ce9f60c364f1e 100644
--- a/app/controllers/projects/boards_controller.rb
+++ b/app/controllers/projects/boards_controller.rb
@@ -8,6 +8,7 @@ class Projects::BoardsController < Projects::ApplicationController
   before_action do
     push_frontend_feature_flag(:board_multi_select, project)
     push_frontend_feature_flag(:apollo_boards, project)
+    push_frontend_feature_flag(:new_graphql_users_autocomplete, project)
     experiment(:prominent_create_board_btn, subject: current_user) do |e|
       e.control {}
       e.candidate {}
diff --git a/ee/app/assets/javascripts/boards/components/board_add_new_column.vue b/ee/app/assets/javascripts/boards/components/board_add_new_column.vue
index 4d832b2c341408a32be9c7b1610b131200689932..22bcd41c2e911b455ab1d4e1cd67adfb75d7d7c8 100644
--- a/ee/app/assets/javascripts/boards/components/board_add_new_column.vue
+++ b/ee/app/assets/javascripts/boards/components/board_add_new_column.vue
@@ -32,6 +32,7 @@ import groupBoardMembersQuery from '~/boards/graphql/group_board_members.query.g
 import projectBoardMembersQuery from '~/boards/graphql/project_board_members.query.graphql';
 import { setError } from '~/boards/graphql/cache_updates';
 import { getListByTypeId } from '~/boards//boards_util';
+import usersAutocompleteQuery from '~/graphql_shared/queries/users_autocomplete.query.graphql';
 import searchIterationQuery from 'ee/issues/list/queries/search_iterations.query.graphql';
 
 export const listTypeInfo = {
@@ -171,15 +172,31 @@ export default {
     },
     assigneesApollo: {
       query() {
+        if (gon.features?.newGraphqlUsersAutocomplete) {
+          return usersAutocompleteQuery;
+        }
+
         if (this.boardType === BoardType.project) {
           return projectBoardMembersQuery;
         }
         return groupBoardMembersQuery;
       },
       variables() {
+        if (gon.features?.newGraphqlUsersAutocomplete) {
+          return {
+            fullPath: this.fullPath,
+            search: this.searchTerm,
+            isProject: this.boardType === BoardType.project,
+          };
+        }
+
         return { ...this.baseVariables, search: this.searchTerm };
       },
       update(data) {
+        if (gon.features?.newGraphqlUsersAutocomplete) {
+          return data[this.boardType]?.autocompleteUsers;
+        }
+
         return data.workspace.assignees.nodes.map(({ user }) => user);
       },
       skip() {
diff --git a/ee/app/assets/javascripts/boards/stores/actions.js b/ee/app/assets/javascripts/boards/stores/actions.js
index 42ec99c92dfaa0b5f5c918822b0ae2501e0392ad..d168e4021a5c5a05bc0d51e84f2b91cbc4fc2b09 100644
--- a/ee/app/assets/javascripts/boards/stores/actions.js
+++ b/ee/app/assets/javascripts/boards/stores/actions.js
@@ -13,6 +13,7 @@ import projectBoardMembersQuery from '~/boards/graphql/project_board_members.que
 import actionsCE from '~/boards/stores/actions';
 import * as typesCE from '~/boards/stores/mutation_types';
 import { TYPENAME_ITERATION, TYPENAME_ITERATIONS_CADENCE } from '~/graphql_shared/constants';
+import usersAutocompleteQuery from '~/graphql_shared/queries/users_autocomplete.query.graphql';
 import { getIdFromGraphQLId, convertToGraphQLId } from '~/graphql_shared/utils';
 import { TYPE_EPIC, WORKSPACE_GROUP, WORKSPACE_PROJECT } from '~/issues/constants';
 import { fetchPolicies } from '~/lib/graphql';
@@ -649,6 +650,21 @@ export default {
       throw new Error('Unknown board type');
     }
 
+    if (gon.features?.newGraphqlUsersAutocomplete) {
+      return gqlClient
+        .query({
+          query: usersAutocompleteQuery,
+          variables: { ...variables, isProject: boardType === WORKSPACE_PROJECT },
+        })
+        .then(({ data }) => {
+          commit(types.RECEIVE_ASSIGNEES_SUCCESS, data[boardType]?.autocompleteUsers);
+        })
+        .catch((e) => {
+          commit(types.RECEIVE_ASSIGNEES_FAILURE);
+          throw e;
+        });
+    }
+
     return gqlClient
       .query({
         query,
diff --git a/spec/features/boards/board_filters_spec.rb b/spec/features/boards/board_filters_spec.rb
index 006b7ce45d4f4261118e46cfaf6189719fb2b28e..bfed6e338aedeaf2c57851ddf7829bd73d49ae40 100644
--- a/spec/features/boards/board_filters_spec.rb
+++ b/spec/features/boards/board_filters_spec.rb
@@ -3,9 +3,9 @@
 require 'spec_helper'
 
 RSpec.describe 'Issue board filters', :js, feature_category: :team_planning do
-  let_it_be(:project) { create(:project, :repository) }
+  let_it_be(:group) { create(:group) }
+  let_it_be(:project) { create(:project, :repository, group: group) }
   let_it_be(:user) { create(:user) }
-  let_it_be(:board) { create(:board, project: project) }
   let_it_be(:project_label) { create(:label, project: project, title: 'Label') }
   let_it_be(:milestone_1) { create(:milestone, project: project, due_date: 3.days.from_now) }
   let_it_be(:milestone_2) { create(:milestone, project: project, due_date: Date.tomorrow) }
@@ -21,166 +21,210 @@
   let(:filter_first_suggestion) { find('.gl-filtered-search-suggestion-list').first('.gl-filtered-search-suggestion') }
   let(:filter_submit) { find('.gl-search-box-by-click-search-button') }
 
-  before do
-    stub_feature_flags(apollo_boards: false)
-    project.add_maintainer(user)
-    sign_in(user)
+  context 'for a project board' do
+    let_it_be(:board) { create(:board, project: project) }
 
-    visit_project_board
-  end
-
-  shared_examples 'loads all the users when opened' do
-    it 'and submit one as filter', :aggregate_failures do
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
+    before do
+      stub_feature_flags(apollo_boards: false)
+      project.add_maintainer(user)
+      sign_in(user)
 
+      visit project_board_path(project, board)
       wait_for_requests
+    end
 
-      expect_filtered_search_dropdown_results(filter_dropdown, 4)
+    shared_examples 'loads all the users when opened' do
+      it 'and submit one as filter', :aggregate_failures do
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
 
-      click_on user.username
-      filter_submit.click
+        wait_for_requests
 
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
-      expect(find('.board-card')).to have_content(issue.title)
-    end
-  end
+        expect_filtered_search_dropdown_results(filter_dropdown, 3)
 
-  describe 'filters by assignee' do
-    before do
-      set_filter('assignee')
-    end
+        click_on user.username
+        filter_submit.click
 
-    it_behaves_like 'loads all the users when opened', quarantine: 'https://gitlab.com/gitlab-org/gitlab/-/issues/351426' do
-      let(:issue) { issue_2 }
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
+        expect(find('.board-card')).to have_content(issue.title)
+      end
     end
-  end
 
-  describe 'filters by author' do
-    before do
-      set_filter('author')
-    end
+    describe 'filters by assignee' do
+      before do
+        set_filter('assignee')
+      end
 
-    it_behaves_like 'loads all the users when opened' do
-      let(:issue) { issue_1 }
+      it_behaves_like 'loads all the users when opened', quarantine: 'https://gitlab.com/gitlab-org/gitlab/-/issues/351426' do
+        let(:issue) { issue_2 }
+      end
     end
-  end
 
-  describe 'filters by label' do
-    before do
-      set_filter('label')
+    describe 'filters by author' do
+      before do
+        set_filter('author')
+      end
+
+      it_behaves_like 'loads all the users when opened' do
+        let(:issue) { issue_1 }
+      end
     end
 
-    it 'loads all the labels when opened and submit one as filter', :aggregate_failures do
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
+    describe 'filters by label' do
+      before do
+        set_filter('label')
+      end
 
-      expect_filtered_search_dropdown_results(filter_dropdown, 3)
+      it 'loads all the labels when opened and submit one as filter', :aggregate_failures do
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
 
-      filter_dropdown.click_on project_label.title
-      filter_submit.click
+        expect_filtered_search_dropdown_results(filter_dropdown, 3)
 
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
-      expect(find('.board-card')).to have_content(issue_2.title)
-    end
-  end
+        filter_dropdown.click_on project_label.title
+        filter_submit.click
 
-  describe 'filters by releases' do
-    before do
-      set_filter('release')
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
+        expect(find('.board-card')).to have_content(issue_2.title)
+      end
     end
 
-    it 'loads all the releases when opened and submit one as filter', :aggregate_failures do
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
+    describe 'filters by releases' do
+      before do
+        set_filter('release')
+      end
 
-      expect_filtered_search_dropdown_results(filter_dropdown, 2)
+      it 'loads all the releases when opened and submit one as filter', :aggregate_failures do
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
 
-      click_on release.tag
-      filter_submit.click
+        expect_filtered_search_dropdown_results(filter_dropdown, 2)
 
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
-      expect(find('.board-card')).to have_content(issue_1.title)
-    end
-  end
+        click_on release.tag
+        filter_submit.click
 
-  describe 'filters by confidentiality' do
-    before do
-      filter_input.click
-      filter_input.set("confidential:")
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
+        expect(find('.board-card')).to have_content(issue_1.title)
+      end
     end
 
-    it 'loads all the confidentiality options when opened and submit one as filter', :aggregate_failures do
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
+    describe 'filters by confidentiality' do
+      before do
+        filter_input.click
+        filter_input.set("confidential:")
+      end
 
-      expect_filtered_search_dropdown_results(filter_dropdown, 2)
+      it 'loads all the confidentiality options when opened and submit one as filter', :aggregate_failures do
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
 
-      filter_dropdown.click_on 'Yes'
-      filter_submit.click
+        expect_filtered_search_dropdown_results(filter_dropdown, 2)
 
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
-      expect(find('.board-card')).to have_content(issue_2.title)
-    end
-  end
+        filter_dropdown.click_on 'Yes'
+        filter_submit.click
 
-  describe 'filters by milestone' do
-    before do
-      set_filter('milestone')
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
+        expect(find('.board-card')).to have_content(issue_2.title)
+      end
     end
 
-    it 'loads all the milestones when opened and submit one as filter', :aggregate_failures do
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
+    describe 'filters by milestone' do
+      before do
+        set_filter('milestone')
+      end
 
-      expect_filtered_search_dropdown_results(filter_dropdown, 6)
-      expect(filter_dropdown).to have_content('None')
-      expect(filter_dropdown).to have_content('Any')
-      expect(filter_dropdown).to have_content('Started')
-      expect(filter_dropdown).to have_content('Upcoming')
+      it 'loads all the milestones when opened and submit one as filter', :aggregate_failures do
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
 
-      dropdown_nodes = page.find_all('.gl-filtered-search-suggestion-list > .gl-filtered-search-suggestion')
+        expect_filtered_search_dropdown_results(filter_dropdown, 6)
+        expect(filter_dropdown).to have_content('None')
+        expect(filter_dropdown).to have_content('Any')
+        expect(filter_dropdown).to have_content('Started')
+        expect(filter_dropdown).to have_content('Upcoming')
 
-      expect(dropdown_nodes[4]).to have_content(milestone_2.title)
-      expect(dropdown_nodes.last).to have_content(milestone_1.title)
+        dropdown_nodes = page.find_all('.gl-filtered-search-suggestion-list > .gl-filtered-search-suggestion')
 
-      click_on milestone_1.title
-      filter_submit.click
+        expect(dropdown_nodes[4]).to have_content(milestone_2.title)
+        expect(dropdown_nodes.last).to have_content(milestone_1.title)
 
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
+        click_on milestone_1.title
+        filter_submit.click
+
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
+      end
     end
-  end
 
-  describe 'filters by reaction emoji' do
-    before do
-      set_filter('my-reaction')
+    describe 'filters by reaction emoji' do
+      before do
+        set_filter('my-reaction')
+      end
+
+      it 'loads all the emojis when opened and submit one as filter', :aggregate_failures do
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
+
+        expect_filtered_search_dropdown_results(filter_dropdown, 3)
+
+        click_on 'thumbsup'
+        filter_submit.click
+
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
+        expect(find('.board-card')).to have_content(issue_1.title)
+      end
     end
 
-    it 'loads all the emojis when opened and submit one as filter', :aggregate_failures do
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 2)
+    describe 'filters by type' do
+      let_it_be(:incident) { create(:incident, project: project) }
 
-      expect_filtered_search_dropdown_results(filter_dropdown, 3)
+      before do
+        set_filter('type')
+      end
 
-      click_on 'thumbsup'
-      filter_submit.click
+      it 'loads all the types when opened and submit one as filter', :aggregate_failures do
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 3)
 
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
-      expect(find('.board-card')).to have_content(issue_1.title)
+        expect_filtered_search_dropdown_results(filter_dropdown, 2)
+
+        click_on 'Incident'
+        filter_submit.click
+
+        expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
+        expect(find('.board-card')).to have_content(incident.title)
+      end
     end
   end
 
-  describe 'filters by type' do
-    let_it_be(:incident) { create(:incident, project: project) }
+  context 'for a group board' do
+    let_it_be(:board) { create(:board, group: group) }
+
+    let_it_be(:child_project_member) { create(:user).tap { |u| project.add_maintainer(u) } }
 
     before do
-      set_filter('type')
+      stub_feature_flags(apollo_boards: false)
+
+      group.add_maintainer(user)
+      sign_in(user)
     end
 
-    it 'loads all the types when opened and submit one as filter', :aggregate_failures do
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 3)
+    context 'when filtering by assignee' do
+      it 'includes descendant project members in autocomplete' do
+        visit group_board_path(group, board)
+        wait_for_requests
+
+        set_filter('assignee')
 
-      expect_filtered_search_dropdown_results(filter_dropdown, 2)
+        expect(page).to have_css('.gl-filtered-search-suggestion', text: child_project_member.name)
+      end
 
-      click_on 'Incident'
-      filter_submit.click
+      context 'when new_graphql_users_autocomplete is disabled' do
+        before do
+          stub_feature_flags(new_graphql_users_autocomplete: false)
+        end
 
-      expect(find('.board:nth-child(1)')).to have_selector('.board-card', count: 1)
-      expect(find('.board-card')).to have_content(incident.title)
+        it 'does not include descendant project members in autocomplete' do
+          visit group_board_path(group, board)
+          wait_for_requests
+
+          set_filter('assignee')
+
+          expect(page).not_to have_css('.gl-filtered-search-suggestion', text: child_project_member.name)
+        end
+      end
     end
   end
 
@@ -193,9 +237,4 @@ def set_filter(filter)
   def expect_filtered_search_dropdown_results(filter_dropdown, count)
     expect(filter_dropdown).to have_selector('.gl-dropdown-item', count: count)
   end
-
-  def visit_project_board
-    visit project_board_path(project, board)
-    wait_for_requests
-  end
 end