diff --git a/CHANGELOG.txt b/CHANGELOG.txt
index 323f6ef72f..27f71e5707 100644
--- a/CHANGELOG.txt
+++ b/CHANGELOG.txt
@@ -41,6 +41,7 @@ Changelog
  * Revise alignment and spacing of form fields and sections (Thibaud Colas)
  * Update Wagtail’s type scale so StreamField block labels and field labels are the same size (Thibaud Colas)
  * Allow customising the `search_fields` and search backend via SnippetViewSet (Sage Abdullah)
+ * Style comments as per page editor design, in side panel (Karl Hobley, Thibaud Colas)
  * Fix: Ensure `label_format` on StructBlock gracefully handles missing variables (Aadi jindal)
  * Fix: Adopt a no-JavaScript and more accessible solution for the 'Reset to default' switch to Gravatar when editing user profile (Loveth Omokaro)
  * Fix: Ensure `Site.get_site_root_paths` works on cache backends that do not preserve Python objects (Jaap Roes)
diff --git a/client/scss/components/_form-side.scss b/client/scss/components/_form-side.scss
index b0c02eb340..545fbf01d1 100644
--- a/client/scss/components/_form-side.scss
+++ b/client/scss/components/_form-side.scss
@@ -53,7 +53,7 @@
   }
 
   &__close-button {
-    @apply w-text-primary w-absolute w-left-3 w-top-3 hover:w-text-primary-200 w-bg-white w-p-3 w-hidden w-transition;
+    @apply w-text-primary w-absolute w-left-3 w-top-3 hover:w-text-primary-200 w-bg-white w-p-3 w-transition;
 
     .icon {
       @apply w-w-4 w-h-4;
@@ -93,10 +93,6 @@
     @apply w-w-0 w-h-0 w-opacity-0 w-absolute w-pointer-events-none;
   }
 
-  &--open .form-side__close-button {
-    @apply w-block;
-  }
-
   &__panel {
     @apply w-px-5 xl:w-px-10 w-py-4 w-w-full w-h-full w-overflow-y-auto w-scrollbar-thin;
   }
diff --git a/client/src/components/CommentApp/components/Comment/index.tsx b/client/src/components/CommentApp/components/Comment/index.tsx
index 172a994c0d..a59dfdb156 100644
--- a/client/src/components/CommentApp/components/Comment/index.tsx
+++ b/client/src/components/CommentApp/components/Comment/index.tsx
@@ -411,7 +411,7 @@ export default class CommentComponent extends React.Component<CommentProps> {
           {gettext('Are you sure?')}
           <button
             type="button"
-            className="comment__button"
+            className="comment__button button button-small"
             onClick={onClickCancel}
           >
             {gettext('Cancel')}
diff --git a/client/src/components/CommentApp/components/Comment/style.scss b/client/src/components/CommentApp/components/Comment/style.scss
index 503df7d3b8..9e51ca3636 100644
--- a/client/src/components/CommentApp/components/Comment/style.scss
+++ b/client/src/components/CommentApp/components/Comment/style.scss
@@ -1,43 +1,23 @@
 .comment {
   @include box;
 
-  width: calc(100vw - 40px);
-  max-width: calc(100vw - 19%);
+  width: 300px;
   display: block;
   transition: top 0.5s ease 0s, inset-inline-end 0.5s ease 0s,
     height 0.5s ease 0s;
   pointer-events: auto;
   padding-bottom: 0;
-  inset-inline-end: -2000px;
-  background-color: theme('colors.white.DEFAULT');
-
-  @include media-breakpoint-up(sm) {
-    width: calc(100vw - 40px);
-    max-width: 400px;
-    inset-inline-start: initial;
-  }
-
-  @include media-breakpoint-up(md) {
-    max-width: 200px;
-    inset-inline-end: 0;
-  }
-
-  @include media-breakpoint-up(lg) {
-    max-width: 275px;
-  }
+  inset-inline-end: 0;
 
   &--focused {
-    inset-inline-end: 35px;
-
-    @include media-breakpoint-up(md) {
-      inset-inline-end: 50px;
-    }
+    inset-inline-end: 30px;
   }
 
   &__text {
     color: $color-box-text;
-    font-size: 13px;
-    line-height: 19px;
+    font-weight: 400;
+    font-size: 16px;
+    line-height: 150%;
     margin-bottom: 0;
     padding-top: 10px;
     padding-bottom: 10px;
@@ -53,11 +33,11 @@
 
   &--mode-creating form {
     border-top: 0;
-    margin-top: 10px;
+    margin-top: 12px;
   }
 
   &--mode-editing form {
-    margin-top: 10px;
+    margin-top: 12px;
   }
 
   &--mode-deleting &__text {
@@ -76,13 +56,13 @@
 
   &__actions,
   &__reply-actions {
-    padding-bottom: 10px;
+    padding-bottom: 20px;
   }
 
   &__actions &__button,
   &__reply-actions &__button {
     margin-inline-end: 10px;
-    margin-top: 10px;
+    margin-top: 12px;
   }
 
   &__confirm-delete &__button {
diff --git a/client/src/components/CommentApp/components/CommentHeader/style.scss b/client/src/components/CommentApp/components/CommentHeader/style.scss
index a67feed45f..0ec05b748a 100644
--- a/client/src/components/CommentApp/components/CommentHeader/style.scss
+++ b/client/src/components/CommentApp/components/CommentHeader/style.scss
@@ -16,8 +16,10 @@
     ); // Leave room for actions to the right and avatar to the left
     margin: 0;
     margin-inline-start: 45px;
-    font-size: 11px;
-    line-height: 15px;
+    font-weight: 600;
+    font-size: 14px;
+    line-height: 130%;
+    color: theme('colors.primary.DEFAULT');
   }
 
   &__date {
diff --git a/client/src/components/CommentApp/components/CommentReply/style.scss b/client/src/components/CommentApp/components/CommentReply/style.scss
index e40e624186..acfc71c0b0 100644
--- a/client/src/components/CommentApp/components/CommentReply/style.scss
+++ b/client/src/components/CommentApp/components/CommentReply/style.scss
@@ -6,8 +6,9 @@
 
   &__text {
     color: $color-box-text;
-    font-size: 13px;
-    line-height: 19px;
+    font-weight: 400;
+    font-size: 16px;
+    line-height: 150%;
     margin-bottom: 0;
     padding-top: 10px;
     padding-bottom: 10px;
diff --git a/client/src/components/CommentApp/main.scss b/client/src/components/CommentApp/main.scss
index cacb8dd623..9245c67a24 100644
--- a/client/src/components/CommentApp/main.scss
+++ b/client/src/components/CommentApp/main.scss
@@ -1,16 +1,14 @@
 @import '../../../scss/settings/variables';
 
-$color-comment-separator: theme('colors.grey.100');
+$color-comment-separator: theme('colors.grey.200');
 
 $color-box-background: $color-white;
-$color-box-border: $color-grey-3;
-$color-box-border-focused: $color-grey-2;
+$color-box-background-focused: theme('colors.grey.50');
+$color-box-border: theme('colors.grey.150');
+$color-box-border-focused: theme('colors.grey.200');
 $color-box-text: $color-black;
-$color-textarea-background: theme('colors.grey.50');
-$color-textarea-border: $color-input-border;
-$color-textarea-placeholder-text: $color-grey-2;
 $box-border-radius: 5px;
-$box-padding: 10px;
+$box-padding: 20px;
 
 @mixin focus-outline {
   outline: $color-focus-outline solid 3px;
@@ -18,28 +16,28 @@ $box-padding: 10px;
 
 @mixin box {
   background-color: $color-box-background;
-  border: 1px solid $color-box-border;
   padding: $box-padding;
-  font-size: 11px;
   border-radius: $box-border-radius;
   color: $color-box-text;
+  border: 1px solid $color-box-border;
 
   &--focused {
+    background-color: $color-box-background-focused;
+    border: 1px solid $color-box-border-focused;
     box-shadow: 3px 2px 3px -1px theme('colors.black-10');
   }
 
   textarea {
-    font-family: $font-sans;
     margin: 0;
-    padding: 10px;
+    padding: 12px;
     width: 100%;
-    background-color: $color-textarea-background;
-    border: 1px solid $color-textarea-border;
+    background-color: $color-white;
+    border: 1px solid $color-input-border;
     border-radius: 5px;
     color: $color-box-text;
 
     &::placeholder {
-      color: $color-textarea-placeholder-text;
+      color: theme('colors.grey.400');
       opacity: 1;
     }
   }
@@ -89,12 +87,10 @@ $box-padding: 10px;
   border-radius: 3px;
   color: $color-teal;
   cursor: pointer;
-  font-family: inherit;
-  font-size: 12px;
-  font-weight: bold;
-  height: 25px;
-  padding-inline-start: 5px;
-  padding-inline-end: 5px;
+  font-weight: 700;
+  height: 30px;
+  padding-inline-start: 10px;
+  padding-inline-end: 10px;
 
   &--primary {
     color: $color-white;
@@ -119,13 +115,10 @@ $box-padding: 10px;
 }
 
 .comments-list {
-  width: 400px;
   position: absolute;
-  top: 30px;
-  inset-inline-end: 35px;
-  z-index: 95;
-  font-family: $font-sans;
-  pointer-events: none;
+  top: 20px;
+  inset-inline-end: 20px;
+  z-index: calc(theme('zIndex.header') + 5);
 }
 
 // stylelint-disable no-invalid-position-at-import-rule
diff --git a/client/src/components/CommentApp/main.tsx b/client/src/components/CommentApp/main.tsx
index 60d5dc9861..d8d8049f69 100644
--- a/client/src/components/CommentApp/main.tsx
+++ b/client/src/components/CommentApp/main.tsx
@@ -1,4 +1,4 @@
-import React from 'react';
+import React, { useCallback } from 'react';
 import ReactDOM from 'react-dom';
 import { createStore } from 'redux';
 
@@ -21,7 +21,6 @@ import {
   selectComments,
   selectCommentsForContentPathFactory,
   selectCommentFactory,
-  selectEnabled,
   selectFocused,
   selectIsDirty,
   selectCommentCount,
@@ -70,17 +69,59 @@ const getAuthor = (
   };
 };
 
-function renderCommentsUi(
-  store: Store,
-  layout: LayoutController,
-  comments: Comment[],
-): React.ReactElement {
+interface CommentListingProps {
+  store: Store;
+  layout: LayoutController;
+  comments: Comment[];
+}
+
+function CommentListing({
+  store,
+  layout,
+  comments,
+}: CommentListingProps): React.ReactElement {
   const state = store.getState();
-  const { commentsEnabled, user, currentTab } = state.settings;
+  const { user, currentTab } = state.settings;
   const { focusedComment, forceFocus } = state.comments;
+  const commentsListRef = React.useRef<HTMLOListElement | null>(null);
+  // Update the position of the comments listing as the window scrolls to keep the comments in line with the content
+  const updateScroll = useCallback(
+    (e: Event) => {
+      if (!commentsListRef.current) {
+        return;
+      }
+
+      if (
+        e.type === 'scroll' &&
+        !document.querySelector('.form-side--comments')
+      ) {
+        return;
+      }
+
+      const scrollContainer = document.querySelector('.content');
+      const top = scrollContainer?.getBoundingClientRect().top;
+      commentsListRef.current.style.top = `${top}px`;
+    },
+    [commentsListRef],
+  );
   let commentsToRender = comments;
 
-  if (!commentsEnabled || !user) {
+  React.useEffect(() => {
+    const root = document.querySelector('#main');
+    const commentSidePanel = document.querySelector(
+      '[data-side-panel="comments"]',
+    );
+
+    root?.addEventListener('scroll', updateScroll);
+    commentSidePanel?.addEventListener('show', updateScroll);
+
+    return () => {
+      root?.removeEventListener('scroll', updateScroll);
+      commentSidePanel?.removeEventListener('show', updateScroll);
+    };
+  }, []);
+
+  if (!user) {
     commentsToRender = [];
   }
   // Hide all resolved/deleted comments
@@ -99,7 +140,11 @@ function renderCommentsUi(
       isVisible={layout.getCommentVisible(currentTab, comment.localId)}
     />
   ));
-  return <ol className="comments-list">{commentsRendered}</ol>;
+  return (
+    <ol ref={commentsListRef} className="comments-list">
+      {commentsRendered}
+    </ol>
+  );
   /* eslint-enable react/no-danger */
 }
 
@@ -115,13 +160,13 @@ export class CommentApp {
 
   selectors = {
     selectComments,
-    selectEnabled,
     selectFocused,
     selectIsDirty,
     selectCommentCount,
   };
 
   actions = commentActionFunctions;
+  activationHandlers: (() => void)[] = [];
 
   constructor() {
     this.store = createStore(reducer, {
@@ -189,12 +234,12 @@ export class CommentApp {
     return commentId;
   }
 
-  setVisible(visible: boolean) {
-    this.store.dispatch(
-      updateGlobalSettings({
-        commentsEnabled: visible,
-      }),
-    );
+  activate() {
+    this.activationHandlers.forEach((handler) => handler());
+  }
+
+  onActivate(handler: () => void) {
+    this.activationHandlers.push(handler);
   }
 
   invalidateContentPath(contentPath: string) {
@@ -255,7 +300,11 @@ export class CommentApp {
       }
 
       ReactDOM.render(
-        renderCommentsUi(this.store, this.layout, commentList),
+        <CommentListing
+          store={this.store}
+          layout={this.layout}
+          comments={commentList}
+        />,
         element,
         () => {
           // Render again if layout has changed (eg, a comment was added, deleted or resized)
@@ -263,7 +312,11 @@ export class CommentApp {
           this.layout.refreshDesiredPositions(state.settings.currentTab);
           if (this.layout.refreshLayout()) {
             ReactDOM.render(
-              renderCommentsUi(this.store, this.layout, commentList),
+              <CommentListing
+                store={this.store}
+                layout={this.layout}
+                comments={commentList}
+              />,
               element,
             );
           }
diff --git a/client/src/components/CommentApp/selectors/index.ts b/client/src/components/CommentApp/selectors/index.ts
index 163344c6ce..b685dd1176 100644
--- a/client/src/components/CommentApp/selectors/index.ts
+++ b/client/src/components/CommentApp/selectors/index.ts
@@ -27,8 +27,6 @@ export function selectCommentFactory(localId: number) {
   });
 }
 
-export const selectEnabled = (state: State) => state.settings.commentsEnabled;
-
 export const selectIsDirty = createSelector(
   selectComments,
   selectRemoteCommentCount,
diff --git a/client/src/components/CommentApp/state/settings.ts b/client/src/components/CommentApp/state/settings.ts
index dbcc7b8357..a6a47d7286 100644
--- a/client/src/components/CommentApp/state/settings.ts
+++ b/client/src/components/CommentApp/state/settings.ts
@@ -5,7 +5,6 @@ import { update } from './utils';
 
 export interface SettingsState {
   user: Author | null;
-  commentsEnabled: boolean;
   currentTab: string | null;
 }
 
@@ -14,7 +13,6 @@ export type SettingsStateUpdate = Partial<SettingsState>;
 // Reducer with initial state
 export const INITIAL_STATE: SettingsState = {
   user: null,
-  commentsEnabled: false,
   currentTab: null,
 };
 
diff --git a/client/src/components/Draftail/CommentableEditor/CommentableEditor.scss b/client/src/components/Draftail/CommentableEditor/CommentableEditor.scss
index 0398a5fb42..1397fbccb0 100644
--- a/client/src/components/Draftail/CommentableEditor/CommentableEditor.scss
+++ b/client/src/components/Draftail/CommentableEditor/CommentableEditor.scss
@@ -1,3 +1,11 @@
+.Draftail-CommentControl {
+  display: none;
+
+  .tab-content--comments-enabled & {
+    display: block;
+  }
+}
+
 .Draftail-CommentControl .Draftail-ToolbarButton {
   color: theme('colors.secondary.100');
 
diff --git a/client/src/components/Draftail/CommentableEditor/CommentableEditor.test.tsx b/client/src/components/Draftail/CommentableEditor/CommentableEditor.test.tsx
index eccd219bb9..69f5db7f3b 100644
--- a/client/src/components/Draftail/CommentableEditor/CommentableEditor.test.tsx
+++ b/client/src/components/Draftail/CommentableEditor/CommentableEditor.test.tsx
@@ -5,7 +5,6 @@ import { createEditorStateFromRaw } from 'draftail';
 import { DraftInlineStyleType, EditorState, SelectionState } from 'draft-js';
 
 import { CommentApp } from '../../CommentApp/main';
-import { updateGlobalSettings } from '../../CommentApp/actions/settings';
 import { newComment } from '../../CommentApp/state/comments';
 import { noop } from '../../../utils/noop';
 
@@ -137,20 +136,12 @@ describe('CommentableEditor', () => {
     commentApp = new CommentApp();
   });
   it('has control', () => {
-    commentApp.setVisible(true);
     const editor = mount(getEditorComponent(commentApp));
     const controls = editor.find('DraftailEditor').prop('controls');
     expect(controls).toHaveLength(1);
     expect(controls[0].inline).toBeTruthy();
     editor.unmount();
   });
-  it('has no control when comments disabled', () => {
-    commentApp.store.dispatch(updateGlobalSettings({ commentsEnabled: false }));
-    const editor = mount(getEditorComponent(commentApp));
-    const controls = editor.find('DraftailEditor').prop('controls');
-    expect(controls).toHaveLength(0);
-    editor.unmount();
-  });
   it('can update comment positions', () => {
     commentApp.store.dispatch(
       commentApp.actions.addComment(
diff --git a/client/src/components/Draftail/CommentableEditor/CommentableEditor.tsx b/client/src/components/Draftail/CommentableEditor/CommentableEditor.tsx
index fe165118b9..29a6b4c3e8 100644
--- a/client/src/components/Draftail/CommentableEditor/CommentableEditor.tsx
+++ b/client/src/components/Draftail/CommentableEditor/CommentableEditor.tsx
@@ -335,6 +335,9 @@ function getCommentControl(
           </>
         }
         onClick={() => {
+          // Open the comments side panel
+          commentApp.activate();
+
           onChange(
             addNewComment(getEditorState(), fieldNode, commentApp, contentPath),
           );
@@ -467,7 +470,6 @@ function getCommentDecorator(commentApp: CommentApp) {
       return null;
     }
 
-    const enabled = useSelector(commentApp.selectors.selectEnabled);
     const blockKey: BlockKey = children[0].props.block.getKey();
     const start: number = children[0].props.start;
 
@@ -490,10 +492,6 @@ function getCommentDecorator(commentApp: CommentApp) {
       return undefined; // eslint demands an explicit return here
     }, [commentId, annotationNode, blockKey]);
 
-    if (!enabled) {
-      return children;
-    }
-
     const onClick = () => {
       // Ensure the comment will appear alongside the current block
       if (!commentId) {
@@ -668,7 +666,6 @@ function CommentableEditor({
     [commentApp],
   );
   const comments = useSelector(commentsSelector, shallowEqual);
-  const enabled = useSelector(commentApp.selectors.selectEnabled);
   const focusedId = useSelector(commentApp.selectors.selectFocused);
 
   const ids = useMemo(
@@ -688,7 +685,6 @@ function CommentableEditor({
 
   const previousFocused = usePrevious(focusedId);
   const previousIds = usePrevious(ids);
-  const previousEnabled = usePrevious(enabled);
   useEffect(() => {
     // Only trigger a focus-related rerender if the current focused comment is inside the field, or the previous one was
     const validFocusChange =
@@ -700,7 +696,6 @@ function CommentableEditor({
 
     if (
       !validFocusChange &&
-      previousEnabled === enabled &&
       (previousIds === ids ||
         (previousIds.length === ids.length &&
           previousIds.every((value, index) => value === ids[index])))
@@ -731,7 +726,7 @@ function CommentableEditor({
       ),
     );
     setUniqueStyleId((id) => (id + 1) % 200);
-  }, [focusedId, enabled, inlineStyles, ids, editorState]);
+  }, [focusedId, inlineStyles, ids, editorState]);
 
   useEffect(() => {
     // if there are any comments without annotations, we need to add them to the EditorState
@@ -806,9 +801,7 @@ function CommentableEditor({
         setEditorState(newEditorState);
       }}
       editorState={editorState}
-      controls={
-        enabled ? controls.concat([{ inline: CommentControl }]) : controls
-      }
+      controls={controls.concat([{ inline: CommentControl }])}
       inlineStyles={inlineStyles.concat(commentStyles)}
       plugins={plugins.concat([
         {
@@ -840,7 +833,10 @@ function CommentableEditor({
             handleArrowAtContentEnd(getEditorState(), setEditorState, 'RTL');
           },
           handleKeyCommand: (command: string, state: EditorState) => {
-            if (enabled && command === 'comment') {
+            if (command === 'comment') {
+              // Open the comments side panel
+              commentApp.activate();
+
               const selection = state.getSelection();
               const content = state.getCurrentContent();
               if (selection.isCollapsed()) {
@@ -869,9 +865,6 @@ function CommentableEditor({
             return 'not-handled';
           },
           customStyleFn: (styleSet: DraftInlineStyle) => {
-            if (!enabled) {
-              return undefined;
-            }
             // Use of casting in this function is due to issue #1563 in immutable-js, which causes operations like
             // map and filter to lose type information on the results. It should be fixed in v4: when we upgrade,
             // this casting should be removed
diff --git a/client/src/entrypoints/admin/comments.js b/client/src/entrypoints/admin/comments.js
index 5cb711a74a..b263b17f5c 100644
--- a/client/src/entrypoints/admin/comments.js
+++ b/client/src/entrypoints/admin/comments.js
@@ -56,18 +56,15 @@ window.comments = (() => {
      * @param {number} localId - the localId of the comment to subscribe to
      */
     subscribeToUpdates(localId) {
-      const { selectFocused, selectEnabled } = commentApp.selectors;
+      const { selectFocused } = commentApp.selectors;
       const selectComment = commentApp.utils.selectCommentFactory(localId);
       const store = commentApp.store;
       const initialState = store.getState();
       let focused = selectFocused(initialState) === localId;
-      let shown = selectEnabled(initialState);
       if (focused) {
         this.onFocus();
       }
-      if (shown) {
-        this.show();
-      }
+      this.show();
       this.unsubscribe = store.subscribe(() => {
         const state = store.getState();
         const comment = selectComment(state);
@@ -83,14 +80,6 @@ window.comments = (() => {
           }
           focused = nowFocused;
         }
-        if (shown !== selectEnabled(state)) {
-          if (shown) {
-            this.hide();
-          } else {
-            this.show();
-          }
-          shown = selectEnabled(state);
-        }
       });
       this.setOnClickHandler(localId);
     }
@@ -125,6 +114,9 @@ window.comments = (() => {
 
     setOnClickHandler(localId) {
       this.node.addEventListener('click', () => {
+        // Open the comments side panel
+        commentApp.activate();
+
         commentApp.store.dispatch(
           commentApp.actions.setFocusedComment(localId, {
             updatePinnedComment: true,
@@ -163,7 +155,6 @@ window.comments = (() => {
         throw new MissingElementError(annotationTemplateNode);
       }
       this.annotationTemplateNode = annotationTemplateNode;
-      this.updateVisibility(false);
     }
 
     register() {
@@ -171,19 +162,14 @@ window.comments = (() => {
         // The widget has no valid contentpath, skip subscriptions
         return undefined;
       }
-      const { selectEnabled } = commentApp.selectors;
       const initialState = commentApp.store.getState();
-      let currentlyEnabled = selectEnabled(initialState);
       const selectCommentsForContentPath =
         commentApp.utils.selectCommentsForContentPathFactory(this.contentpath);
       let currentComments = selectCommentsForContentPath(initialState);
-      this.updateVisibility(currentComments.length === 0 && currentlyEnabled);
       const unsubscribeWidget = commentApp.store.subscribe(() => {
         const state = commentApp.store.getState();
         const newComments = selectCommentsForContentPath(state);
-        const newEnabled = selectEnabled(state);
         const commentsChanged = currentComments !== newComments;
-        const enabledChanged = currentlyEnabled !== newEnabled;
         if (commentsChanged) {
           // Add annotations for any new comments
           currentComments = newComments;
@@ -195,14 +181,6 @@ window.comments = (() => {
               annotation.subscribeToUpdates(comment.localId);
             });
         }
-        if (enabledChanged || commentsChanged) {
-          // If comments have been enabled or disabled, or the comments have changed
-          // check whether to show the widget (if comments are enabled and there are no existing comments)
-          currentlyEnabled = newEnabled;
-          this.updateVisibility(
-            currentComments.length === 0 && currentlyEnabled,
-          );
-        }
       });
       initialState.comments.comments.forEach((comment) => {
         // Add annotations for any comments already in the store
@@ -218,11 +196,14 @@ window.comments = (() => {
         annotation.subscribeToUpdates(localId);
       };
       this.commentAdditionNode.addEventListener('click', () => {
+        // Open the comments side panel
+        commentApp.activate();
+
         // Make the widget button clickable to add a comment
         addComment();
       });
       this.fieldNode.addEventListener('keyup', (e) => {
-        if (currentlyEnabled && isCommentShortcut(e)) {
+        if (isCommentShortcut(e)) {
           if (currentComments.length === 0) {
             addComment();
           } else {
@@ -239,19 +220,6 @@ window.comments = (() => {
       return unsubscribeWidget; // TODO: listen for widget deletion and use this
     }
 
-    updateVisibility(newShown) {
-      if (newShown === this.shown) {
-        return;
-      }
-      this.shown = newShown;
-
-      if (!this.shown) {
-        this.commentAdditionNode.classList.add('u-hidden');
-      } else {
-        this.commentAdditionNode.classList.remove('u-hidden');
-      }
-    }
-
     getAnnotationForComment() {
       const annotationNode = this.annotationTemplateNode.cloneNode(true);
       annotationNode.id = '';
@@ -276,38 +244,13 @@ window.comments = (() => {
     }
   }
 
-  function onNextEnable(fn) {
-    // Run a function once, when comments are enabled
-    const { selectEnabled } = commentApp.selectors;
-    const getEnabled = () => selectEnabled(commentApp.store.getState());
-    let enabled = getEnabled();
-    if (enabled) {
-      // If we're starting off enabled, run the function immediately
-      fn();
-      return;
-    }
-    const unsubscribe = commentApp.store.subscribe(() => {
-      // Otherwise, subscribe to updates and run the function when comments change to enabled
-      const newEnabled = getEnabled();
-      if (newEnabled && !enabled) {
-        enabled = newEnabled;
-        unsubscribe();
-        fn();
-      }
-    });
-  }
-
   function initAddCommentButton(buttonElement) {
-    const initWidget = () => {
-      const widget = new FieldLevelCommentWidget({
-        fieldNode: buttonElement.closest('[data-contentpath]'),
-        commentAdditionNode: buttonElement,
-        annotationTemplateNode: document.querySelector('#comment-icon'),
-      });
-      widget.register();
-    };
-    // Our template node may not exist yet - let's hold off until comments are loaded and enabled
-    onNextEnable(initWidget);
+    const widget = new FieldLevelCommentWidget({
+      fieldNode: buttonElement.closest('[data-contentpath]'),
+      commentAdditionNode: buttonElement,
+      annotationTemplateNode: document.querySelector('#comment-icon'),
+    });
+    widget.register();
   }
 
   function initCommentsInterface(formElement) {
@@ -348,42 +291,21 @@ window.comments = (() => {
       });
     }
 
-    // Show/hide comments when the side panel is opened/closed
-    const commentsSidePanel = document.querySelector(
-      '[data-side-panel="comments"]',
-    );
+    // Show comments app
     const commentNotifications = formElement.querySelector(
       '[data-comment-notifications]',
     );
+    commentNotifications.hidden = false;
     const tabContentElement = formElement.querySelector('.tab-content');
+    tabContentElement.classList.add('tab-content--comments-enabled');
 
-    const updateCommentVisibility = (visible) => {
-      // Show/hide comments
-      commentApp.setVisible(visible);
-
-      // Add/Remove tab-nav--comments-enabled class. This changes the size of streamfields
-      if (visible) {
-        tabContentElement.classList.add('tab-content--comments-enabled');
-        if (commentNotifications) {
-          commentNotifications.hidden = false;
-        }
-      } else {
-        tabContentElement.classList.remove('tab-content--comments-enabled');
-        if (commentNotifications) {
-          commentNotifications.hidden = true;
-        }
-      }
-    };
-
-    if (commentsSidePanel) {
-      commentsSidePanel.addEventListener('show', () => {
-        updateCommentVisibility(true);
-      });
-
-      commentsSidePanel.addEventListener('hide', () => {
-        updateCommentVisibility(false);
-      });
-    }
+    // Open the comments panel whenever the comment app is activated by a user clicking on an "Add comment" widget on the form.
+    const commentSidePanel = document.querySelector(
+      '[data-side-panel="comments"]',
+    );
+    commentApp.onActivate(() => {
+      commentSidePanel.dispatchEvent(new Event('open'));
+    });
 
     // Keep number of comments up to date with comment app
     const commentToggle = document.querySelector(
diff --git a/client/src/includes/sidePanel.js b/client/src/includes/sidePanel.js
index 97144ff72a..3155bda890 100644
--- a/client/src/includes/sidePanel.js
+++ b/client/src/includes/sidePanel.js
@@ -43,14 +43,7 @@ export default function initSidePanel() {
     if (panelName && !selectedPanel) return;
 
     // Open / close side panel
-
-    // HACK: For now, the comments will show without the side-panel opening.
-    // They will later be updated so that they render inside the side panel.
-    // We couldn't implement this for Wagtail 3.0 as the existing field styling
-    // renders the "Add comment" button on the right hand side, and this gets
-    // covered up by the side panel.
-
-    if (panelName === '' || panelName === 'comments') {
+    if (panelName === '') {
       sidePanelWrapper.classList.remove('form-side--open');
       sidePanelWrapper.removeAttribute('aria-labelledby');
     } else {
@@ -129,6 +122,14 @@ export default function initSidePanel() {
     }
   };
 
+  // Open the side panel if the 'open' custom event is triggered on the side panel
+  // This is allows panels to be opened with JavaScript without hacking the toggle
+  document.querySelectorAll('[data-side-panel]').forEach((panel) => {
+    panel.addEventListener('open', () => {
+      setPanel(panel.dataset.sidePanel);
+    });
+  });
+
   document.querySelectorAll('[data-side-panel-toggle]').forEach((toggle) => {
     toggle.addEventListener('click', () => {
       togglePanel(toggle.dataset.sidePanelToggle);
diff --git a/docs/releases/5.0.md b/docs/releases/5.0.md
index ee75929004..1e6fc1817d 100644
--- a/docs/releases/5.0.md
+++ b/docs/releases/5.0.md
@@ -80,6 +80,7 @@ Those improvements were implemented by Albina Starykova as part of an [Outreachy
  * Revise alignment and spacing of form fields and sections (Thibaud Colas)
  * Update Wagtail’s type scale so StreamField block labels and field labels are the same size (Thibaud Colas)
  * Allow customising the `search_fields` and search backend via SnippetViewSet (Sage Abdullah)
+ * Style comments as per page editor design, in side panel (Karl Hobley, Thibaud Colas)
 
 ### Bug fixes
 
diff --git a/wagtail/admin/templates/wagtailadmin/pages/create.html b/wagtail/admin/templates/wagtailadmin/pages/create.html
index b8991e180f..f6887fd559 100644
--- a/wagtail/admin/templates/wagtailadmin/pages/create.html
+++ b/wagtail/admin/templates/wagtailadmin/pages/create.html
@@ -5,7 +5,6 @@
 {% block titletag %}{% blocktrans trimmed with page_type=content_type.model_class.get_verbose_name %}New {{ page_type }}{% endblocktrans %}{% endblock %}
 
 {% block content %}
-    <div id="comments"></div>
 
     <div class="w-sticky w-top-0 w-z-header">
         {% include 'wagtailadmin/shared/headers/page_create_header.html' %}
diff --git a/wagtail/admin/templates/wagtailadmin/pages/edit.html b/wagtail/admin/templates/wagtailadmin/pages/edit.html
index 3defa1a136..684fe684cd 100644
--- a/wagtail/admin/templates/wagtailadmin/pages/edit.html
+++ b/wagtail/admin/templates/wagtailadmin/pages/edit.html
@@ -6,7 +6,6 @@
 {% block bodyclass %}{% if page.live %}page-is-live{% endif %} {% if page_locked %}content-locked{% endif %}{% endblock %}
 
 {% block content %}
-    <div id="comments"></div>
     {% page_permissions page as page_perms %}
 
     <div class="w-sticky w-top-0 w-z-header">
diff --git a/wagtail/admin/templates/wagtailadmin/shared/field.html b/wagtail/admin/templates/wagtailadmin/shared/field.html
index 21bbd717e3..d61b48746f 100644
--- a/wagtail/admin/templates/wagtailadmin/shared/field.html
+++ b/wagtail/admin/templates/wagtailadmin/shared/field.html
@@ -73,7 +73,7 @@
             {% endblock %}
 
             {% if show_add_comment_button %}
-                <button class="w-field__comment-button w-field__comment-button--add u-hidden" type="button" data-component="add-comment-button" data-comment-add aria-label="{% trans 'Add comment' %}" {% if label_for %}aria-describedby="{{ label_id }}"{% endif %}>
+                <button class="w-field__comment-button w-field__comment-button--add" type="button" data-component="add-comment-button" data-comment-add aria-label="{% trans 'Add comment' %}" {% if label_for %}aria-describedby="{{ label_id }}"{% endif %}>
                     {% icon name="comment-add" %}
                     {% icon name="comment-add-reversed" %}
                 </button>
diff --git a/wagtail/admin/templates/wagtailadmin/shared/side_panels/comments.html b/wagtail/admin/templates/wagtailadmin/shared/side_panels/comments.html
index e69de29bb2..034e080f9a 100644
--- a/wagtail/admin/templates/wagtailadmin/shared/side_panels/comments.html
+++ b/wagtail/admin/templates/wagtailadmin/shared/side_panels/comments.html
@@ -0,0 +1 @@
+<div id="comments"></div>