diff --git a/src/browser/base/content/browser-verticaltabs.js b/src/browser/base/content/browser-verticaltabs.js
index a9ec5f22..501926ed 100644
--- a/src/browser/base/content/browser-verticaltabs.js
+++ b/src/browser/base/content/browser-verticaltabs.js
@@ -5,6 +5,47 @@
 
 const VERTICAL_TABS_POSITION = 'pulse.tabs.vertical'
 const VERTICAL_TABS_COLLAPSE = 'pulse.tabs.vertical.collapse'
+const VERTICAL_TABS_WIDTH = 'pulse.tabs.vertical.width'
+
+/**
+ * @param {HTMLElement} toInsertAfter This is the element that I want to insert content after
+ * @param {HTMLElement} toInsert The element to insert
+ *
+ * @throws {Error} If the element you want me to base insertions on has no parent
+ */
+function insertAfter(toInsertAfter, toInsert) {
+  const parent = toInsertAfter.parentNode
+
+  if (!parent) {
+    throw new Error(
+      'The element you want me to base insertions on has no parent'
+    )
+  }
+
+  if (toInsertAfter.nextSibling) {
+    parent.insertBefore(toInsert, toInsertAfter.nextSibling)
+  } else {
+    parent.appendChild(toInsert)
+  }
+}
+
+/**
+ * Replace a tag with another tag with a different name
+ * @param {string} tagName The new tag name
+ * @param {HTMLElement?} initialTag The tag to be changed
+ */
+function changeXULTagName(tagName, initialTag) {
+  if (!initialTag) return
+  if (initialTag.tagName == tagName) return
+
+  const newParent = document.createXULElement(tagName)
+
+  for (const attr of initialTag.attributes)
+    newParent.setAttribute(attr.name, attr.value)
+  while (initialTag.firstChild) newParent.appendChild(initialTag.firstChild)
+
+  initialTag.replaceWith(newParent)
+}
 
 var VerticalTabs = {
   /**
@@ -35,6 +76,13 @@ var VerticalTabs = {
     return document.getElementById('browser')
   },
 
+  /**
+   * @return {HTMLElement?}
+   */
+  get splitter() {
+    return document.getElementById('verticaltabs-splitter')
+  },
+
   /**
    * @return {Boolean}
    */
@@ -48,6 +96,8 @@ var VerticalTabs = {
   tabBrowserTabs: null,
 
   _initialized: false,
+  /** @type {MutationObserver?} */
+  _widthObserver: null,
 
   init() {
     if (this._initialized) {
@@ -79,9 +129,40 @@ var VerticalTabs = {
       .querySelector('#TabsToolbar .toolbar-items')
       ?.setAttribute('align', 'start')
 
-    document
-      .getElementById('TabsToolbar')
-      ?.setAttribute('collapse', this.browserCollapseTabs ? 'true' : 'false')
+    this.tabsToolbar?.setAttribute(
+      'collapse',
+      this.browserCollapseTabs ? 'true' : 'false'
+    )
+    this.tabsToolbar?.removeAttribute('flex')
+    changeXULTagName('vbox', this.tabsToolbar)
+
+    this._widthObserver = new MutationObserver(this._mutationObserverCallback)
+    if (this.tabsToolbar)
+      this._widthObserver.observe(this.tabsToolbar, { attributes: true })
+
+    this.tabsToolbar?.setAttribute(
+      'width',
+      Services.prefs.getIntPref(VERTICAL_TABS_WIDTH, 200)
+    )
+    if (this.tabsToolbar)
+      this.tabsToolbar.style.width = `${Services.prefs.getIntPref(
+        VERTICAL_TABS_WIDTH,
+        200
+      )}px`
+
+    if (!this.splitter) {
+      const separator = document.createXULElement('splitter')
+      separator.setAttribute('id', 'verticaltabs-splitter')
+      separator.setAttribute(
+        'class',
+        'chromeclass-extrachrome verticaltabs-splitter'
+      )
+      separator.setAttribute('resizebefore', 'none')
+      separator.setAttribute('resizeafter', 'sibling')
+
+      const tabs = this.tabsToolbar
+      if (tabs) tabs.parentElement?.insertBefore(separator, tabs)
+    }
   },
 
   disableVerticalTabs() {
@@ -96,6 +177,39 @@ var VerticalTabs = {
     document
       .querySelector('#TabsToolbar .toolbar-items')
       ?.setAttribute('align', 'end')
+
+    if (this.tabsToolbar) {
+      changeXULTagName('toolbar', this.tabsToolbar)
+      this.tabsToolbar.setAttribute('flex', '1')
+      // Reset the resize value, or else the tabs will end up squished
+      this.tabsToolbar.style.width = ''
+    }
+
+    if (this.splitter) {
+      this.splitter.remove()
+    }
+
+    if (this._widthObserver) {
+      this._widthObserver.disconnect()
+      this._widthObserver = null
+    }
+  },
+
+  /**
+   * @param {MutationRecord[]} mutationsList
+   * @param {MutationObserver} _observer
+   */
+  _mutationObserverCallback(mutationsList, _observer) {
+    for (const mutation of mutationsList) {
+      if (mutation.type === 'attributes' && mutation.attributeName == 'width') {
+        const tabsToolbar = document.getElementById('TabsToolbar')
+
+        Services.prefs.setIntPref(
+          VERTICAL_TABS_WIDTH,
+          parseInt(tabsToolbar?.getAttribute('width') || '100')
+        )
+      }
+    }
   },
 
   /**
diff --git a/src/browser/themes/pulse/vertical_tabs.css b/src/browser/themes/pulse/vertical_tabs.css
index 46ebf7cc..be08bb7c 100644
--- a/src/browser/themes/pulse/vertical_tabs.css
+++ b/src/browser/themes/pulse/vertical_tabs.css
@@ -3,6 +3,10 @@
  * License, v. 2.0. If a copy of the MPL was not distributed with this
  * file, You can obtain one at http://mozilla.org/MPL/2.0/.
  */
+:root {
+  --vertical-tabs-max-width: 350px;
+}
+
 #browser #TabsToolbar .titlebar-spacer,
 #browser #TabsToolbar .titlebar-buttonbox-container,
 #browser #TabsToolbar #alltabs-button {
@@ -10,14 +14,29 @@
 }
 
 #navigator-toolbox-background[verticaltabs='true'] #titlebar {
-    display: none;
+  display: none;
 }
 
 #browser #TabsToolbar {
   background-color: -moz-Dialog;
-  max-width: 350px;
+  max-width: var(--vertical-tabs-max-width);
+  -moz-box-ordinal-group: 0;
+}
+
+#browser #TabsToolbar:not([collapse='true']) {
+  min-width: 76px;
+}
 
-  transition: all 200ms ease-in-out;
+#browser #TabsToolbar[collapse='true'] {
+  max-width: calc(
+    16px + 2 * var(--inline-tab-padding) + 2 * var(--tab-block-margin)
+  );
+}
+
+/** On collapse hover of tabs or splitter, the max width should increase again */
+#browser #TabsToolbar[collapse='true']:hover,
+#verticaltabs-splitter:hover ~ #TabsToolbar[collapse='true'] {
+  max-width: var(--vertical-tabs-max-width);
 }
 
 #browser #TabsToolbar:-moz-lwtheme {
@@ -36,9 +55,6 @@
   /* Stops the tabs from getting squished or stretched */
   min-height: unset;
   max-height: var(--tab-min-height);
-
-  /* Animate tabs out vertically */
-  transition: min-height 100ms ease-out, max-height 100ms ease-out;
 }
 
 /* Put the new tab button on the bottom */
@@ -93,12 +109,15 @@
   margin-inline-start: none;
 }
 
-#browser #TabsToolbar[collapse='true']:not(:hover) {
-  max-width: calc(
-    16px + 2 * var(--inline-tab-padding) + 2 * var(--tab-block-margin)
-  );
+#browser #TabsToolbar[collapse='true'] .tabbrowser-tab {
+  /* Animate tabs out vertically */
+  transition: min-height 100ms ease-out, max-height 100ms ease-out;
+}
+
+#verticaltabs-splitter {
+  -moz-box-ordinal-group: 1;
 }
 
 :root[sizemode='fullscreen'] #browser #TabsToolbar {
-    display: none;
-}
\ No newline at end of file
+  display: none;
+}