diff --git a/ghost/admin/app/components/gh-koenig-editor-lexical.hbs b/ghost/admin/app/components/gh-koenig-editor-lexical.hbs
index 50d763684a..2933f6000c 100644
--- a/ghost/admin/app/components/gh-koenig-editor-lexical.hbs
+++ b/ghost/admin/app/components/gh-koenig-editor-lexical.hbs
@@ -59,18 +59,22 @@
 
             {{#if (feature 'editorSubtitle')}}
                 <GhTextarea
-                    @class="gh-editor-subtitle"
-                    @placeholder="Add a post excerpt..."
+                    @class={{concat "gh-editor-subtitle " (if @excerptErrorMessage "red")}}
+                    @placeholder="Add a subtitle..."
                     @shouldFocus={{false}}
                     @tabindex="1"
                     @autoExpand=".gh-koenig-editor"
                     @value={{readonly this.excerpt}}
-                    @input={{this.updateExcerpt}}
-                    @focus-out={{optional @blurExcerpt}}
+                    @input={{this.onExcerptInput}}
                     @keyDown={{this.onExcerptKeydown}}
-                    data-test-editor-subhead-input={{true}}
+                    data-test-textarea="subtitle"
                 />
-                <hr class="gh-editor-title-divider">
+                {{#if @excerptErrorMessage}}
+                    <div class="gh-editor-subtitle-error" data-test-error="subtitle">
+                        {{@excerptErrorMessage}}
+                    </div>
+                {{/if}}
+                <hr class="gh-editor-title-divider {{if @excerptErrorMessage "gh-editor-title-divider-error" ""}}">
             {{/if}}
         </div>
 
diff --git a/ghost/admin/app/components/gh-koenig-editor-lexical.js b/ghost/admin/app/components/gh-koenig-editor-lexical.js
index 4836f7c80f..643dc8cdf4 100644
--- a/ghost/admin/app/components/gh-koenig-editor-lexical.js
+++ b/ghost/admin/app/components/gh-koenig-editor-lexical.js
@@ -153,18 +153,8 @@ export default class GhKoenigEditorReactComponent extends Component {
     // Subhead ("excerpt") Actions -------------------------------------------
 
     @action
-    updateExcerpt(event) {
-        this.args.onExcerptChange?.(event.target.value);
-    }
-
-    @action
-    focusExcerpt() {
-        this.args.onExcerptFocus?.();
-    }
-
-    @action
-    blurExcerpt() {
-        this.args.onExcerptBlur?.();
+    onExcerptInput(event) {
+        this.args.setExcerpt?.(event.target.value);
     }
 
     @action
diff --git a/ghost/admin/app/controllers/lexical-editor.js b/ghost/admin/app/controllers/lexical-editor.js
index b0240287bb..d42bdd6c36 100644
--- a/ghost/admin/app/controllers/lexical-editor.js
+++ b/ghost/admin/app/controllers/lexical-editor.js
@@ -285,8 +285,13 @@ export default class LexicalEditorController extends Controller {
     }
 
     @action
-    updateExcerptScratch(excerpt) {
-        this.set('post.customExcerptScratch', excerpt);
+    updateExcerpt(excerpt) {
+        this.post.customExcerpt = excerpt;
+        this.post.validate({property: 'customExcerpt'});
+    }
+
+    get excerptErrorMessage() {
+        return this.post.errors.errorsFor('customExcerpt')?.[0]?.message;
     }
 
     // updates local willPublish/Schedule values, does not get applied to
diff --git a/ghost/admin/app/styles/layouts/editor.css b/ghost/admin/app/styles/layouts/editor.css
index 6b0f8545c8..e7c0e1bef5 100644
--- a/ghost/admin/app/styles/layouts/editor.css
+++ b/ghost/admin/app/styles/layouts/editor.css
@@ -811,10 +811,22 @@ body[data-user-is-dragging] .gh-editor-feature-image-dropzone {
     border: none !important;
 }
 
+.gh-editor-subtitle-error {
+    margin-top: .8rem;
+    color: var(--red-d1);
+    font-size: 1.4rem;
+    font-weight: 400;
+}
+
 .gh-editor-title-divider {
     margin: 1.6rem 0 4.8rem;
 }
 
+.gh-editor-title-divider-error {
+    margin: .4rem 0 4.8rem;
+    border-top: 1px solid var(--red);
+}
+
 .gh-editor .tk-indicator {
     position: absolute;
     top: 15px;
diff --git a/ghost/admin/app/templates/lexical-editor.hbs b/ghost/admin/app/templates/lexical-editor.hbs
index 8db8681d03..77847a47eb 100644
--- a/ghost/admin/app/templates/lexical-editor.hbs
+++ b/ghost/admin/app/templates/lexical-editor.hbs
@@ -62,11 +62,12 @@
             <GhKoenigEditorLexical
                 @title={{readonly this.post.titleScratch}}
                 @excerpt={{readonly this.post.customExcerpt}}
+                @setExcerpt={{this.updateExcerpt}}
+                @excerptErrorMessage={{this.excerptErrorMessage}}
                 @titleAutofocus={{this.shouldFocusTitle}}
                 @titlePlaceholder={{concat (capitalize this.post.displayName) " title"}}
                 @titleHasTk={{this.titleHasTk}}
                 @onTitleChange={{this.updateTitleScratch}}
-                @onExcerptChange={{this.updateExcerptScratch}}
                 @onTitleBlur={{perform this.saveTitleTask}}
                 @body={{readonly this.post.lexicalScratch}}
                 @bodyPlaceholder={{concat "Begin writing your " this.post.displayName "..."}}
@@ -95,6 +96,7 @@
                 }}
                 @postType={{this.post.displayName}}
                 @registerAPI={{this.registerEditorAPI}}
+                @savePostTask={{this.savePostTask}}
             />
 
             <div class="gh-editor-wordcount-container">
diff --git a/ghost/admin/app/validators/post.js b/ghost/admin/app/validators/post.js
index ec32addd34..90f8a2e96d 100644
--- a/ghost/admin/app/validators/post.js
+++ b/ghost/admin/app/validators/post.js
@@ -62,7 +62,11 @@ export default BaseValidator.create({
 
     customExcerpt(model) {
         if (!validator.isLength(model.customExcerpt || '', 0, 300)) {
-            model.errors.add('customExcerpt', 'Excerpt cannot be longer than 300 characters.');
+            if (model.feature.editorSubtitle) {
+                model.errors.add('customExcerpt', 'Please keep the subtitle under 300 characters.');
+            } else {
+                model.errors.add('customExcerpt', 'Excerpt cannot be longer than 300 characters.');
+            }
             this.invalidate();
         }
     },
diff --git a/ghost/admin/tests/acceptance/editor-test.js b/ghost/admin/tests/acceptance/editor-test.js
index 612f2e7ddc..841164eafa 100644
--- a/ghost/admin/tests/acceptance/editor-test.js
+++ b/ghost/admin/tests/acceptance/editor-test.js
@@ -5,6 +5,7 @@ import {authenticateSession, invalidateSession} from 'ember-simple-auth/test-sup
 import {beforeEach, describe, it} from 'mocha';
 import {blur, click, currentRouteName, currentURL, fillIn, find, findAll, triggerEvent, typeIn} from '@ember/test-helpers';
 import {datepickerSelect} from 'ember-power-datepicker/test-support';
+import {enableLabsFlag} from '../helpers/labs-flag';
 import {expect} from 'chai';
 import {selectChoose} from 'ember-power-select/test-support';
 import {setupApplicationTest} from 'ember-mocha';
@@ -490,6 +491,38 @@ describe('Acceptance: Editor', function () {
             ).to.equal(0);
         });
 
+        it('handles in-editor excerpt update and validation', async function () {
+            enableLabsFlag(this.server, 'editorSubtitle');
+
+            let post = this.server.create('post', {authors: [author], customExcerpt: 'Existing excerpt'});
+
+            await visit(`/editor/post/${post.id}`);
+
+            expect(find('[data-test-textarea="subtitle"]'), 'initial textarea').to.be.visible;
+            expect(find('[data-test-textarea="subtitle"]'), 'initial textarea').to.have.value('Existing excerpt');
+
+            await fillIn('[data-test-textarea="subtitle"]', 'New excerpt');
+            expect(find('[data-test-textarea="subtitle"]'), 'updated textarea').to.have.value('New excerpt');
+
+            await triggerEvent('[data-test-textarea="subtitle"]', 'keydown', {
+                key: 's',
+                keyCode: 83, // s
+                metaKey: ctrlOrCmd === 'command',
+                ctrlKey: ctrlOrCmd === 'ctrl'
+            });
+
+            expect(post.customExcerpt, 'saved excerpt').to.equal('New excerpt');
+
+            await fillIn('[data-test-textarea="subtitle"]', Array(302).join('a'));
+
+            expect(find('[data-test-error="subtitle"]'), 'subtitle error').to.exist;
+            expect(find('[data-test-error="subtitle"]')).to.have.trimmed.text('Please keep the subtitle under 300 characters.');
+
+            await fillIn('[data-test-textarea="subtitle"]', Array(300).join('a'));
+
+            expect(find('[data-test-error="subtitle"]'), 'subtitle error').to.not.exist;
+        });
+
         // https://github.com/TryGhost/Ghost/issues/11786
         // NOTE: Flaky test with moving to Lexical editor, skipping for now
         it.skip('save shortcut works when tags/authors field is focused', async function () {