diff --git a/app/assets/javascripts/contextual_sidebar.js b/app/assets/javascripts/contextual_sidebar.js
index 46b68ebe158..cd20dde2951 100644
--- a/app/assets/javascripts/contextual_sidebar.js
+++ b/app/assets/javascripts/contextual_sidebar.js
@@ -28,7 +28,7 @@ export default class ContextualSidebar {
     this.$closeSidebar.on('click', () => this.toggleSidebarNav(false));
     this.$overlay.on('click', () => this.toggleSidebarNav(false));
     this.$sidebarToggle.on('click', () => {
-      const value = !this.$sidebar.hasClass('sidebar-icons-only');
+      const value = !this.$sidebar.hasClass('sidebar-collapsed-desktop');
       this.toggleCollapsedSidebar(value);
     });
 
@@ -43,16 +43,16 @@ export default class ContextualSidebar {
   }
 
   toggleSidebarNav(show) {
-    this.$sidebar.toggleClass('nav-sidebar-expanded', show);
+    this.$sidebar.toggleClass('sidebar-expanded-mobile', show);
     this.$overlay.toggleClass('mobile-nav-open', show);
-    this.$sidebar.removeClass('sidebar-icons-only');
+    this.$sidebar.removeClass('sidebar-collapsed-desktop');
   }
 
   toggleCollapsedSidebar(collapsed) {
     const breakpoint = bp.getBreakpointSize();
 
     if (this.$sidebar.length) {
-      this.$sidebar.toggleClass('sidebar-icons-only', collapsed);
+      this.$sidebar.toggleClass('sidebar-collapsed-desktop', collapsed);
       this.$page.toggleClass('page-with-icon-sidebar', breakpoint === 'sm' ? true : collapsed);
     }
     ContextualSidebar.setCollapsedCookie(collapsed);
diff --git a/app/assets/javascripts/fly_out_nav.js b/app/assets/javascripts/fly_out_nav.js
index 98837c3b2a0..6110d961609 100644
--- a/app/assets/javascripts/fly_out_nav.js
+++ b/app/assets/javascripts/fly_out_nav.js
@@ -21,7 +21,7 @@ let headerHeight = 50;
 
 export const getHeaderHeight = () => headerHeight;
 
-export const isSidebarCollapsed = () => sidebar && sidebar.classList.contains('sidebar-icons-only');
+export const isSidebarCollapsed = () => sidebar && sidebar.classList.contains('sidebar-collapsed-desktop');
 
 export const canShowActiveSubItems = (el) => {
   if (el.classList.contains('active') && !isSidebarCollapsed()) {
diff --git a/app/assets/stylesheets/framework/contextual-sidebar.scss b/app/assets/stylesheets/framework/contextual-sidebar.scss
index b73932eb7e1..26a2db99e0a 100644
--- a/app/assets/stylesheets/framework/contextual-sidebar.scss
+++ b/app/assets/stylesheets/framework/contextual-sidebar.scss
@@ -1,4 +1,6 @@
 .page-with-contextual-sidebar {
+  transition: padding-left $sidebar-transition-duration;
+
   @media (min-width: $screen-md-min) {
     padding-left: $contextual-sidebar-collapsed-width;
   }
@@ -27,8 +29,10 @@
 .context-header {
   position: relative;
   margin-right: 2px;
+  width: $contextual-sidebar-width;
 
   a {
+    transition: padding $sidebar-transition-duration;
     font-weight: $gl-font-weight-bold;
     display: flex;
     align-items: center;
@@ -63,10 +67,10 @@
 }
 
 .nav-sidebar {
+  transition: width $sidebar-transition-duration, left $sidebar-transition-duration;
   position: fixed;
   z-index: 400;
   width: $contextual-sidebar-width;
-  transition: left $sidebar-transition-duration;
   top: $header-height;
   bottom: 0;
   left: 0;
@@ -74,16 +78,15 @@
   box-shadow: inset -2px 0 0 $border-color;
   transform: translate3d(0, 0, 0);
 
-  &:not(.sidebar-icons-only) {
+  &:not(.sidebar-collapsed-desktop) {
     @media (min-width: $screen-sm-min) and (max-width: $screen-md-max) {
       box-shadow: inset -2px 0 0 $border-color,
                   2px 1px 3px $dropdown-shadow-color;
     }
   }
 
-  &.sidebar-icons-only {
-    width: auto;
-    min-width: $contextual-sidebar-collapsed-width;
+  &.sidebar-collapsed-desktop {
+    width: $contextual-sidebar-collapsed-width;
 
     .nav-sidebar-inner-scroll {
       overflow-x: hidden;
@@ -108,12 +111,11 @@
     }
   }
 
-  &.nav-sidebar-expanded {
+  &.sidebar-expanded-mobile {
     left: 0;
   }
 
   a {
-    transition: none;
     text-decoration: none;
   }
 
@@ -126,9 +128,10 @@
     white-space: nowrap;
 
     a {
+      transition: padding $sidebar-transition-duration;
       display: flex;
       align-items: center;
-      padding: 12px 16px;
+      padding: 12px 15px;
       color: $gl-text-color-secondary;
     }
 
@@ -288,7 +291,8 @@
 
       > a {
         margin-left: 4px;
-        padding-left: 12px;
+        // Subtract width of left border on active element
+        padding-left: 11px;
       }
 
       .badge {
@@ -313,6 +317,7 @@
 .toggle-sidebar-button,
 .close-nav-button {
   width: $contextual-sidebar-width - 2px;
+  transition: width $sidebar-transition-duration;
   position: fixed;
   bottom: 0;
   padding: 16px;
@@ -343,20 +348,21 @@
   }
 }
 
+.collapse-text {
+  white-space: nowrap;
+  overflow: hidden;
+}
 
-.sidebar-icons-only {
+.sidebar-collapsed-desktop {
   .context-header {
-    height: 61px;
+    height: 60px;
+    width: $contextual-sidebar-collapsed-width;
 
     a {
       padding: 10px 4px;
     }
   }
 
-  li a {
-    padding: 12px 15px;
-  }
-
   .sidebar-top-level-items > li {
     &.active a {
       padding-left: 12px;
@@ -374,8 +380,8 @@
   }
 
   .toggle-sidebar-button {
-    width: $contextual-sidebar-collapsed-width - 2px;
     padding: 16px;
+    width: $contextual-sidebar-collapsed-width - 2px;
 
     .collapse-text,
     .icon-angle-double-left {
diff --git a/app/assets/stylesheets/framework/variables.scss b/app/assets/stylesheets/framework/variables.scss
index 4f99c27eff1..a6fa96d834c 100644
--- a/app/assets/stylesheets/framework/variables.scss
+++ b/app/assets/stylesheets/framework/variables.scss
@@ -5,10 +5,9 @@ $grid-size: 8px;
 $gutter_collapsed_width: 62px;
 $gutter_width: 290px;
 $gutter_inner_width: 250px;
-$sidebar-transition-duration: .15s;
+$sidebar-transition-duration: .3s;
 $sidebar-breakpoint: 1024px;
 $default-transition-duration: .15s;
-$right-sidebar-transition-duration: .3s;
 $contextual-sidebar-width: 220px;
 $contextual-sidebar-collapsed-width: 50px;
 
diff --git a/app/assets/stylesheets/pages/boards.scss b/app/assets/stylesheets/pages/boards.scss
index 3683afa07de..862ea379cbc 100644
--- a/app/assets/stylesheets/pages/boards.scss
+++ b/app/assets/stylesheets/pages/boards.scss
@@ -57,7 +57,7 @@
   position: relative;
 
   @media (min-width: $screen-sm-min) {
-    transition: width $right-sidebar-transition-duration;
+    transition: width $sidebar-transition-duration;
     width: 100%;
 
     &.is-compact {
@@ -453,8 +453,8 @@
 .right-sidebar.right-sidebar-expanded {
   &.boards-sidebar-slide-enter-active,
   &.boards-sidebar-slide-leave-active {
-    transition: width $right-sidebar-transition-duration,
-                padding $right-sidebar-transition-duration;
+    transition: width $sidebar-transition-duration,
+                padding $sidebar-transition-duration;
   }
 
   &.boards-sidebar-slide-enter,
diff --git a/app/assets/stylesheets/pages/issuable.scss b/app/assets/stylesheets/pages/issuable.scss
index 11ee1232bfe..32f2fa88236 100644
--- a/app/assets/stylesheets/pages/issuable.scss
+++ b/app/assets/stylesheets/pages/issuable.scss
@@ -126,7 +126,7 @@
   top: $header-height;
   bottom: 0;
   right: 0;
-  transition: width $right-sidebar-transition-duration;
+  transition: width $sidebar-transition-duration;
   background: $gray-light;
   z-index: 200;
   overflow: hidden;
diff --git a/app/views/layouts/nav/sidebar/_admin.html.haml b/app/views/layouts/nav/sidebar/_admin.html.haml
index 0ec07605631..cb8db306b56 100644
--- a/app/views/layouts/nav/sidebar/_admin.html.haml
+++ b/app/views/layouts/nav/sidebar/_admin.html.haml
@@ -1,4 +1,4 @@
-.nav-sidebar{ class: ("sidebar-icons-only" if collapsed_sidebar?) }
+.nav-sidebar{ class: ("sidebar-collapsed-desktop" if collapsed_sidebar?) }
   .nav-sidebar-inner-scroll
     .context-header
       = link_to admin_root_path, title: 'Admin Overview' do
diff --git a/app/views/layouts/nav/sidebar/_group.html.haml b/app/views/layouts/nav/sidebar/_group.html.haml
index 0bf318b0b66..0c27b09f7b1 100644
--- a/app/views/layouts/nav/sidebar/_group.html.haml
+++ b/app/views/layouts/nav/sidebar/_group.html.haml
@@ -1,7 +1,7 @@
 - issues = IssuesFinder.new(current_user, group_id: @group.id, state: 'opened').execute
 - merge_requests = MergeRequestsFinder.new(current_user, group_id: @group.id, state: 'opened', non_archived: true).execute
 
-.nav-sidebar{ class: ("sidebar-icons-only" if collapsed_sidebar?) }
+.nav-sidebar{ class: ("sidebar-collapsed-desktop" if collapsed_sidebar?) }
   .nav-sidebar-inner-scroll
     .context-header
       = link_to group_path(@group), title: @group.name do
diff --git a/app/views/layouts/nav/sidebar/_profile.html.haml b/app/views/layouts/nav/sidebar/_profile.html.haml
index 7e23f9c1f05..a5a62a0695f 100644
--- a/app/views/layouts/nav/sidebar/_profile.html.haml
+++ b/app/views/layouts/nav/sidebar/_profile.html.haml
@@ -1,4 +1,4 @@
-.nav-sidebar{ class: ("sidebar-icons-only" if collapsed_sidebar?) }
+.nav-sidebar{ class: ("sidebar-collapsed-desktop" if collapsed_sidebar?) }
   .nav-sidebar-inner-scroll
     .context-header
       = link_to profile_path, title: 'Profile Settings' do
diff --git a/app/views/layouts/nav/sidebar/_project.html.haml b/app/views/layouts/nav/sidebar/_project.html.haml
index 53a9162b703..be39f577ba7 100644
--- a/app/views/layouts/nav/sidebar/_project.html.haml
+++ b/app/views/layouts/nav/sidebar/_project.html.haml
@@ -1,4 +1,4 @@
-.nav-sidebar{ class: ("sidebar-icons-only" if collapsed_sidebar?) }
+.nav-sidebar{ class: ("sidebar-collapsed-desktop" if collapsed_sidebar?) }
   .nav-sidebar-inner-scroll
     - can_edit = can?(current_user, :admin_project, @project)
     .context-header
diff --git a/changelogs/unreleased/35724-animate-sidebar.yml b/changelogs/unreleased/35724-animate-sidebar.yml
new file mode 100644
index 00000000000..5d0b46a23c8
--- /dev/null
+++ b/changelogs/unreleased/35724-animate-sidebar.yml
@@ -0,0 +1,5 @@
+---
+title: Animate contextual sidebar on collapse/expand
+merge_request:
+author:
+type: changed
diff --git a/spec/javascripts/fly_out_nav_spec.js b/spec/javascripts/fly_out_nav_spec.js
index 4f20e31f511..a3fa07d5bc2 100644
--- a/spec/javascripts/fly_out_nav_spec.js
+++ b/spec/javascripts/fly_out_nav_spec.js
@@ -253,7 +253,7 @@ describe('Fly out sidebar navigation', () => {
     it('shows collapsed only sub-items if icon only sidebar', () => {
       const subItems = el.querySelector('.sidebar-sub-level-items');
       const sidebar = document.createElement('div');
-      sidebar.classList.add('sidebar-icons-only');
+      sidebar.classList.add('sidebar-collapsed-desktop');
       subItems.classList.add('is-fly-out-only');
 
       setSidebar(sidebar);
@@ -343,7 +343,7 @@ describe('Fly out sidebar navigation', () => {
 
     it('returns true when active & collapsed sidebar', () => {
       const sidebar = document.createElement('div');
-      sidebar.classList.add('sidebar-icons-only');
+      sidebar.classList.add('sidebar-collapsed-desktop');
       el.classList.add('active');
 
       setSidebar(sidebar);