diff --git a/app/assets/javascripts/vue_merge_request_widget/components/states/ready_to_merge.vue b/app/assets/javascripts/vue_merge_request_widget/components/states/ready_to_merge.vue
index 3ff2488d8787e4b7713cce078bf2e78788ee94ec..f4b65479fa006de2dfab1a201c5e800db9703cb8 100644
--- a/app/assets/javascripts/vue_merge_request_widget/components/states/ready_to_merge.vue
+++ b/app/assets/javascripts/vue_merge_request_widget/components/states/ready_to_merge.vue
@@ -11,6 +11,7 @@ import {
   GlSkeletonLoader,
 } from '@gitlab/ui';
 import { isEmpty, isNil } from 'lodash';
+import * as Sentry from '~/sentry/sentry_browser_wrapper';
 import axios from '~/lib/utils/axios_utils';
 import readyToMergeMixin from 'ee_else_ce/vue_merge_request_widget/mixins/ready_to_merge';
 import readyToMergeQuery from 'ee_else_ce/vue_merge_request_widget/queries/states/ready_to_merge.query.graphql';
@@ -204,6 +205,7 @@ export default {
       editCommitMessage: false,
       isRebaseInProgress: false,
       isRebaseModalVisible: false,
+      relatedLinks: this.mr.relatedLinks,
     };
   },
   computed: {
@@ -377,6 +379,8 @@ export default {
     eventHub.$on('ApprovalUpdated', this.updateGraphqlState);
     eventHub.$on('MRWidgetUpdateRequested', this.updateGraphqlState);
     eventHub.$on('mr.discussion.updated', this.updateGraphqlState);
+
+    this.fetchRelatedLinks();
   },
   beforeDestroy() {
     eventHub.$off('ApprovalUpdated', this.updateGraphqlState);
@@ -584,6 +588,35 @@ export default {
         this.isRebaseInProgress = false;
       }
     },
+    async fetchRelatedLinks() {
+      if (!this.mr.mergeRequestIssueLinksPath) return;
+
+      try {
+        const {
+          data: { issues_links: issuesLinks },
+        } = await axios.get(this.mr.mergeRequestIssueLinksPath);
+
+        if (issuesLinks) {
+          const { closing } = issuesLinks;
+          const mentioned = issuesLinks.mentioned_but_not_closing;
+          const assignToMe = issuesLinks.assign_to_closing;
+          const unassignedCount = issuesLinks.assign_to_closing_count;
+
+          if (closing || mentioned || unassignedCount) {
+            this.relatedLinks = {
+              closing,
+              mentioned,
+              assignToMe,
+              closingCount: issuesLinks.closing_count,
+              mentionedCount: issuesLinks.mentioned_count,
+              unassignedCount,
+            };
+          }
+        }
+      } catch (error) {
+        Sentry.captureException(error);
+      }
+    },
   },
   i18n: {
     mergeCommitTemplateHintText: s__(
@@ -745,11 +778,11 @@ export default {
                     :target-branch="state.targetBranch"
                   />
                 </li>
-                <template v-if="mr.relatedLinks">
+                <template v-if="relatedLinks">
                   <li>
                     <related-links
                       :state="mr.state"
-                      :related-links="mr.relatedLinks"
+                      :related-links="relatedLinks"
                       :show-assign-to-me="false"
                       :diverged-commits-count="mr.divergedCommitsCount"
                       :target-branch-path="mr.targetBranchPath"
diff --git a/app/assets/javascripts/vue_merge_request_widget/stores/mr_widget_store.js b/app/assets/javascripts/vue_merge_request_widget/stores/mr_widget_store.js
index 2729f3d2b560569257b0f17d6d1447f0bfb4ab87..30d19c3adc961033c541433fb981e52092321e4b 100644
--- a/app/assets/javascripts/vue_merge_request_widget/stores/mr_widget_store.js
+++ b/app/assets/javascripts/vue_merge_request_widget/stores/mr_widget_store.js
@@ -266,6 +266,7 @@ export default class MergeRequestStore {
     this.mergeRequestBasicPath = data.merge_request_basic_path;
     this.mergeRequestWidgetPath = data.merge_request_widget_path;
     this.mergeRequestCachedWidgetPath = data.merge_request_cached_widget_path;
+    this.mergeRequestIssueLinksPath = data.merge_request_issue_links_path;
     this.emailPatchesPath = data.email_patches_path;
     this.plainDiffPath = data.plain_diff_path;
     this.mergeCheckPath = data.merge_check_path;
diff --git a/app/controllers/projects/merge_requests/content_controller.rb b/app/controllers/projects/merge_requests/content_controller.rb
index 588fc85ff771d4dcdce9a57a2a6e2a83102d6ceb..164a65cc49415e521ad9e61f969a127d275e47de 100644
--- a/app/controllers/projects/merge_requests/content_controller.rb
+++ b/app/controllers/projects/merge_requests/content_controller.rb
@@ -34,6 +34,14 @@ def cached_widget
     end
   end
 
+  def widget_issue_links
+    respond_to do |format|
+      format.json do
+        render json: serializer(MergeRequests::WidgetIssueLinksEntity)
+      end
+    end
+  end
+
   private
 
   def set_polling_header
diff --git a/app/serializers/merge_request_widget_entity.rb b/app/serializers/merge_request_widget_entity.rb
index cf0fd0b451e71ea1511c4b5092f9ebb73f425194..282d7e19e86598efead64360876eb1bb7f060ad7 100644
--- a/app/serializers/merge_request_widget_entity.rb
+++ b/app/serializers/merge_request_widget_entity.rb
@@ -44,6 +44,10 @@ class MergeRequestWidgetEntity < Grape::Entity
     cached_widget_project_json_merge_request_path(merge_request.target_project, merge_request, format: :json)
   end
 
+  expose :merge_request_issue_links_path, if: ->(mr, _) { !Rails.cache.exist?(['merge_request', mr.id, 'issues_links']) } do |merge_request|
+    widget_issue_links_project_json_merge_request_path(merge_request.target_project, merge_request, format: :json)
+  end
+
   expose :commit_change_content_path do |merge_request|
     commit_change_content_project_merge_request_path(merge_request.project, merge_request)
   end
@@ -114,31 +118,7 @@ class MergeRequestWidgetEntity < Grape::Entity
   # Rendering and redacting Markdown can be expensive. These links are
   # just nice to have in the merge request widget, so only
   # include them if they are explicitly requested on first load.
-  expose :issues_links, if: ->(_, opts) { opts[:issues_links] } do
-    expose :assign_to_closing do |merge_request|
-      presenter(merge_request).assign_to_closing_issues_path
-    end
-
-    expose :assign_to_closing_count do |merge_request|
-      presenter(merge_request).assign_to_closing_issues_count
-    end
-
-    expose :closing do |merge_request|
-      presenter(merge_request).closing_issues_links
-    end
-
-    expose :closing_count do |merge_request|
-      presenter(merge_request).closing_issues.size
-    end
-
-    expose :mentioned_but_not_closing do |merge_request|
-      presenter(merge_request).mentioned_issues_links
-    end
-
-    expose :mentioned_count do |merge_request|
-      presenter(merge_request).mentioned_issues.size
-    end
-  end
+  expose :issues_links, if: ->(_, opts) { opts[:issues_links] }
 
   expose :security_reports_docs_path do |merge_request|
     help_page_path('user/application_security/detect/security_scanning_results.md', anchor: 'merge-request-security-widget')
@@ -174,6 +154,10 @@ def presenter(merge_request)
     @presenters[merge_request] ||= MergeRequestPresenter.new(merge_request, current_user: current_user) # rubocop: disable CodeReuse/Presenter
   end
 
+  def issues_links
+    Rails.cache.read(['merge_request', object.id, 'issues_links'])
+  end
+
   def can_add_ci_config_path?(merge_request)
     merge_request.open? &&
       merge_request.source_branch_exists? &&
diff --git a/app/serializers/merge_requests/widget_issue_links_entity.rb b/app/serializers/merge_requests/widget_issue_links_entity.rb
new file mode 100644
index 0000000000000000000000000000000000000000..27d5dd20251bb2a1831f66c9b33d84b040ceeb48
--- /dev/null
+++ b/app/serializers/merge_requests/widget_issue_links_entity.rb
@@ -0,0 +1,29 @@
+# frozen_string_literal: true
+
+module MergeRequests
+  class WidgetIssueLinksEntity < Grape::Entity
+    include RequestAwareEntity
+    include ::Gitlab::Utils::StrongMemoize
+
+    expose :issues_links
+
+    private
+
+    delegate :current_user, to: :request
+
+    def issues_links
+      presenter = MergeRequestPresenter.new(object, current_user: current_user) # rubocop: disable CodeReuse/Presenter -- Moved from another existing entity
+
+      Rails.cache.fetch(['merge_request', object.id, 'issues_links']) do
+        {
+          assign_to_closing: presenter.assign_to_closing_issues_path,
+          assign_to_closing_count: presenter.assign_to_closing_issues_count,
+          closing: presenter.closing_issues_links,
+          closing_count: presenter.closing_issues.count,
+          mentioned_but_not_closing: presenter.mentioned_issues_links,
+          mentioned_count: presenter.mentioned_issues.count
+        }
+      end
+    end
+  end
+end
diff --git a/app/services/merge_requests/update_service.rb b/app/services/merge_requests/update_service.rb
index 35826707c57e5c212343fab875ba7fad9b3a8c52..4a9755a784abe4fa959693f06794f54d97b80c82 100644
--- a/app/services/merge_requests/update_service.rb
+++ b/app/services/merge_requests/update_service.rb
@@ -37,6 +37,10 @@ def handle_changes(merge_request, options)
 
       if merge_request.previous_changes.include?('title') ||
           merge_request.previous_changes.include?('description')
+        # Delete the issue links cache so that we can update the cache with any new mentioned issues
+        # on the next load of a merge request
+        Rails.cache.delete(['merge_request', merge_request.id, 'issues_links'])
+
         todo_service.update_merge_request(merge_request, current_user, old_mentioned_users)
         handle_title_and_desc_edits(merge_request, merge_request.previous_changes.keys)
       end
diff --git a/app/views/projects/merge_requests/_widget.html.haml b/app/views/projects/merge_requests/_widget.html.haml
index ea3af550a1537713e952b7daa9baed25de510aa0..7ec75dc6f39a1a6ff9029b3b97aa25cdcfa32745 100644
--- a/app/views/projects/merge_requests/_widget.html.haml
+++ b/app/views/projects/merge_requests/_widget.html.haml
@@ -3,7 +3,7 @@
 = javascript_tag do
   :plain
     window.gl = window.gl || {};
-    window.gl.mrWidgetData = #{serialize_issuable(@merge_request, serializer: 'widget', issues_links: true)}
+    window.gl.mrWidgetData = #{serialize_issuable(@merge_request, serializer: 'widget', issues_links: Rails.cache.exist?(['merge_request', @merge_request.id, 'issues_links']))}
 
     window.gl.mrWidgetData.artifacts_endpoint = '#{downloadable_artifacts_project_pipeline_path(@project, artifacts_endpoint_placeholder, format: :json)}';
     window.gl.mrWidgetData.artifacts_endpoint_placeholder = '#{artifacts_endpoint_placeholder}';
diff --git a/config/routes/merge_requests.rb b/config/routes/merge_requests.rb
index 50b0417cea89c83f04a7ec8c4bdf58fe6fb3bdbc..b2627cec3eebe3da4cf5c58c3be97df600564df5 100644
--- a/config/routes/merge_requests.rb
+++ b/config/routes/merge_requests.rb
@@ -32,6 +32,7 @@
       get :diffs_metadata, to: 'merge_requests/diffs#diffs_metadata'
       get :widget, to: 'merge_requests/content#widget'
       get :cached_widget, to: 'merge_requests/content#cached_widget'
+      get :widget_issue_links, to: 'merge_requests/content#widget_issue_links'
     end
 
     scope action: :show do
diff --git a/ee/spec/frontend/vue_merge_request_widget/components/states/mr_widget_ready_to_merge_spec.js b/ee/spec/frontend/vue_merge_request_widget/components/states/mr_widget_ready_to_merge_spec.js
index 66d4b64b3bcddf14a3aaec3c56577c20b094c14b..f32fd979c90637baf7f6158f074f4b9d2cb3b31e 100644
--- a/ee/spec/frontend/vue_merge_request_widget/components/states/mr_widget_ready_to_merge_spec.js
+++ b/ee/spec/frontend/vue_merge_request_widget/components/states/mr_widget_ready_to_merge_spec.js
@@ -1,5 +1,7 @@
 import { GlLink, GlSprintf, GlDisclosureDropdown, GlDisclosureDropdownItem } from '@gitlab/ui';
 import { nextTick } from 'vue';
+import MockAdapter from 'axios-mock-adapter';
+import axios from '~/lib/utils/axios_utils';
 import MergeImmediatelyConfirmationDialog from 'ee/vue_merge_request_widget/components/merge_immediately_confirmation_dialog.vue';
 import MergeTrainRestartTrainConfirmationDialog from 'ee/vue_merge_request_widget/components/merge_train_restart_train_confirmation_dialog.vue';
 import MergeTrainFailedPipelineConfirmationDialog from 'ee/vue_merge_request_widget/components/merge_train_failed_pipeline_confirmation_dialog.vue';
@@ -14,6 +16,7 @@ import {
 
 describe('ReadyToMerge', () => {
   let wrapper;
+  let mock;
   const showMock = jest.fn();
 
   const service = {
@@ -112,6 +115,14 @@ describe('ReadyToMerge', () => {
   const findMergeHelperText = () => wrapper.findByTestId('auto-merge-helper-text');
 
   describe('Merge Immediately Dropdown', () => {
+    beforeEach(() => {
+      mock = new MockAdapter(axios);
+    });
+
+    afterEach(() => {
+      mock.restore();
+    });
+
     it('should return false if auto merge is not available', () => {
       createComponent({
         headPipeline: { id: 'gid://gitlab/Pipeline/1', path: 'path/to/pipeline', active: true },
diff --git a/spec/controllers/projects/merge_requests/content_controller_spec.rb b/spec/controllers/projects/merge_requests/content_controller_spec.rb
index 69edb47fe71f7d631f9c29a36fd651486d98b7ad..cdb5c00b7cbd22b73288ae4c3fb39ecfd418c00c 100644
--- a/spec/controllers/projects/merge_requests/content_controller_spec.rb
+++ b/spec/controllers/projects/merge_requests/content_controller_spec.rb
@@ -84,6 +84,14 @@ def do_request(action = :cached_widget, params = {})
         end
       end
     end
+
+    describe 'GET widget_issue_links' do
+      it 'renders widget issue links entity as json' do
+        do_request(:widget_issue_links)
+
+        expect(response).to match_response_schema('entities/merge_request_widget_issue_links')
+      end
+    end
   end
 
   context 'user does not have access to the project' do
@@ -102,5 +110,13 @@ def do_request(action = :cached_widget, params = {})
         expect(response).to have_gitlab_http_status(:not_found)
       end
     end
+
+    describe 'GET widget_issue_links' do
+      it 'returns 404' do
+        do_request(:widget_issue_links)
+
+        expect(response).to have_gitlab_http_status(:not_found)
+      end
+    end
   end
 end
diff --git a/spec/fixtures/api/schemas/entities/merge_request_widget_issue_links.json b/spec/fixtures/api/schemas/entities/merge_request_widget_issue_links.json
new file mode 100644
index 0000000000000000000000000000000000000000..ed511610bb2431aaaee031a32cc943b2fa0a36a3
--- /dev/null
+++ b/spec/fixtures/api/schemas/entities/merge_request_widget_issue_links.json
@@ -0,0 +1,18 @@
+{
+  "type": "object",
+  "properties": {
+    "issues_links": {
+      "type": "object",
+      "required": ["closing", "mentioned_but_not_closing", "assign_to_closing", "assign_to_closing_count", "closing_count", "mentioned_count"],
+      "properties": {
+        "closing": { "type": "string" },
+        "mentioned_but_not_closing": { "type": "string" },
+        "assign_to_closing": { "type": ["string", "null"] },
+        "assign_to_closing_count": { "type": "integer" },
+        "closing_count": { "type": "integer" },
+        "mentioned_count": { "type": "integer" }
+      },
+      "additionalProperties": false
+    }
+  }
+}
diff --git a/spec/frontend/vue_merge_request_widget/components/states/mr_widget_ready_to_merge_spec.js b/spec/frontend/vue_merge_request_widget/components/states/mr_widget_ready_to_merge_spec.js
index f2a59a246ead80a5fd9e5d889f8d88e73b688b54..c4752143b425a77e589de48abed9d0381280d97f 100644
--- a/spec/frontend/vue_merge_request_widget/components/states/mr_widget_ready_to_merge_spec.js
+++ b/spec/frontend/vue_merge_request_widget/components/states/mr_widget_ready_to_merge_spec.js
@@ -3,6 +3,7 @@ import { GlFormTextarea, GlSprintf } from '@gitlab/ui';
 import VueApollo from 'vue-apollo';
 import produce from 'immer';
 import { createMockSubscription as createMockApolloSubscription } from 'mock-apollo-client';
+import MockAdapter from 'axios-mock-adapter';
 import readyToMergeResponse from 'test_fixtures/graphql/merge_requests/states/ready_to_merge.query.graphql.json';
 import axios from '~/lib/utils/axios_utils';
 import { shallowMountExtended } from 'helpers/vue_test_utils_helper';
@@ -13,6 +14,7 @@ import simplePoll from '~/lib/utils/simple_poll';
 import CommitEdit from '~/vue_merge_request_widget/components/states/commit_edit.vue';
 import CommitMessageDropdown from '~/vue_merge_request_widget/components/states/commit_message_dropdown.vue';
 import ReadyToMerge from '~/vue_merge_request_widget/components/states/ready_to_merge.vue';
+import RelatedLinks from '~/vue_merge_request_widget/components/mr_widget_related_links.vue';
 import SquashBeforeMerge from '~/vue_merge_request_widget/components/states/squash_before_merge.vue';
 import MergeFailedPipelineConfirmationDialog from '~/vue_merge_request_widget/components/states/merge_failed_pipeline_confirmation_dialog.vue';
 import { MWCP_MERGE_STRATEGY } from '~/vue_merge_request_widget/constants';
@@ -68,6 +70,7 @@ const createTestMr = (customConfig) => {
       canMerge: true,
     },
     targetProjectId: 1,
+    mergeRequestIssueLinksPath: '/merge_request/issue_links',
   };
 
   Object.assign(mr, customConfig.mr);
@@ -86,6 +89,7 @@ let service;
 let wrapper;
 let readyToMergeResponseSpy;
 let mockedSubscription;
+let mock;
 
 const createReadyToMergeResponse = (customMr) => {
   return produce(readyToMergeResponse, (draft) => {
@@ -169,6 +173,12 @@ describe('ReadyToMerge', () => {
   beforeEach(() => {
     service = createTestService();
     readyToMergeResponseSpy = jest.fn().mockResolvedValueOnce(readyToMergeResponse);
+
+    mock = new MockAdapter(axios);
+  });
+
+  afterEach(() => {
+    mock.restore();
   });
 
   describe('computed', () => {
@@ -1182,4 +1192,62 @@ describe('ReadyToMerge', () => {
       );
     });
   });
+
+  describe('issue links', () => {
+    describe('when API return issue links', () => {
+      beforeEach(() => {
+        mock.onGet('/merge_request/issue_links').reply(200, {
+          issues_links: {
+            mentioned_but_not_closing: '#1',
+            assign_to_closing: '#1',
+            assign_to_closing_count: 1,
+            closing_count: 1,
+            mentioned_count: 1,
+            closing: 1,
+          },
+        });
+      });
+
+      it('renders related links component', async () => {
+        createComponent();
+
+        await waitForPromises();
+
+        const relatedLinksComponent = wrapper.findComponent(RelatedLinks);
+
+        expect(relatedLinksComponent.exists()).toBe(true);
+        expect(relatedLinksComponent.props('relatedLinks')).toEqual({
+          assignToMe: '#1',
+          closing: 1,
+          closingCount: 1,
+          mentioned: '#1',
+          mentionedCount: 1,
+          unassignedCount: 1,
+        });
+      });
+    });
+
+    describe('when API does not return issue links', () => {
+      beforeEach(() => {
+        mock.onGet('/merge_request/issue_links').reply(200, {
+          issues_links: {
+            mentioned_but_not_closing: '',
+            assign_to_closing: '',
+            assign_to_closing_count: 0,
+            closing_count: 0,
+            mentioned_count: 0,
+            closing: 0,
+          },
+        });
+      });
+
+      it('renders related links component', async () => {
+        createComponent();
+
+        await waitForPromises();
+
+        expect(wrapper.findComponent(RelatedLinks).exists()).toBe(false);
+      });
+    });
+  });
 });
diff --git a/spec/serializers/merge_request_widget_entity_spec.rb b/spec/serializers/merge_request_widget_entity_spec.rb
index e9707265263b2ac568e5f054bed11574e81124cf..453d9a6967fc609e6fada13383a7013e9e2d71c5 100644
--- a/spec/serializers/merge_request_widget_entity_spec.rb
+++ b/spec/serializers/merge_request_widget_entity_spec.rb
@@ -55,7 +55,23 @@
   end
 
   describe 'issues links' do
+    it 'returns nil if cache is empty' do
+      data = described_class.new(resource, request: request, issues_links: true).as_json
+
+      expect(data).to include(:issues_links)
+      expect(data[:issues_links]).to be_nil
+    end
+
     it 'includes issues links when requested' do
+      allow(Rails.cache).to receive(:read).with(['merge_request', resource.id, 'issues_links']).and_return({
+        assign_to_closing: '',
+        assign_to_closing_count: 0,
+        closing: '',
+        mentioned_but_not_closing: '',
+        closing_count: 0,
+        mentioned_count: 0
+      })
+
       data = described_class.new(resource, request: request, issues_links: true).as_json
 
       expect(data).to include(:issues_links)