diff --git a/browser/components/tabbrowser/content/tabs.js b/browser/components/tabbrowser/content/tabs.js
index 676bb0e53d26..24a9df9d99d8 100644
--- a/browser/components/tabbrowser/content/tabs.js
+++ b/browser/components/tabbrowser/content/tabs.js
@@ -41,6 +41,8 @@
 
     #maxTabsPerRow;
     #dragOverCreateGroupTimer;
+    #mustUpdateTabMinHeight = false;
+    #tabMinHeight = 36;
 
     constructor() {
       super();
@@ -92,6 +94,18 @@
         return (!tab.pinned || !arePositioningPinnedTabs()) && tab.visible;
       };
 
+      // Override for performance reasons. This is the size of a single element
+      // that can be scrolled when using mouse wheel scrolling. If we don't do
+      // this then arrowscrollbox computes this value by calling
+      // _getScrollableElements and dividing the box size by that number.
+      // However in the tabstrip case we already know the answer to this as,
+      // when we're overflowing, it is always the same as the tab min width or
+      // height.
+      Object.defineProperty(this.arrowScrollbox, "lineScrollAmount", {
+        get: () =>
+          this.verticalMode ? this.#tabMinHeight : this._tabMinWidthPref,
+      });
+
       this.baseConnect();
 
       this._blockDblClick = false;
@@ -163,6 +177,7 @@
         }
       );
       this.#updateTabMinWidth(this._tabMinWidthPref);
+      this.#updateTabMinHeight();
 
       CustomizableUI.addListener(this);
       this._updateNewTabVisibility();
@@ -202,6 +217,7 @@
       this._positionPinnedTabs();
 
       this.#updateTabMinWidth();
+      this.#updateTabMinHeight();
 
       let indicatorTabs = gBrowser.visibleTabs.filter(tab => {
         return (
@@ -1529,7 +1545,11 @@
         node = this.arrowScrollbox.lastChild;
       }
 
-      return node.before(tab);
+      node.before(tab);
+
+      if (this.#mustUpdateTabMinHeight) {
+        this.#updateTabMinHeight();
+      }
     }
 
     #updateTabMinWidth(val) {
@@ -1544,6 +1564,53 @@
       }
     }
 
+    #updateTabMinHeight() {
+      if (!this.verticalMode || !window.toolbar.visible) {
+        this.#mustUpdateTabMinHeight = false;
+        return;
+      }
+
+      // Find at least one tab we can scroll to.
+      let firstScrollableTab = this.visibleTabs.find(
+        this.arrowScrollbox._canScrollToElement
+      );
+
+      if (!firstScrollableTab) {
+        // If not, we're in a pickle. We should never get here except if we
+        // also don't use the outcome of this work (because there's nothing to
+        // scroll so we don't care about the scrollbox size).
+        // So just set a flag so we re-run once we do have a new tab.
+        this.#mustUpdateTabMinHeight = true;
+        return;
+      }
+
+      let { height } =
+        window.windowUtils.getBoundsWithoutFlushing(firstScrollableTab);
+
+      // Use the current known height or a sane default.
+      this.#tabMinHeight = height || 36;
+
+      // The height we got may be incorrect if a flush is pending so re-check it after
+      // a flush completes.
+      window
+        .promiseDocumentFlushed(() => {})
+        .then(
+          () => {
+            height =
+              window.windowUtils.getBoundsWithoutFlushing(
+                firstScrollableTab
+              ).height;
+
+            if (height) {
+              this.#tabMinHeight = height;
+            }
+          },
+          () => {
+            /* ignore errors */
+          }
+        );
+    }
+
     get _isCustomizing() {
       return document.documentElement.hasAttribute("customizing");
     }
@@ -1791,6 +1858,7 @@
     uiDensityChanged() {
       this._positionPinnedTabs();
       this._updateCloseButtons();
+      this.#updateTabMinHeight();
       this._handleTabSelect(true);
     }
 
diff --git a/browser/components/tabbrowser/test/browser/tabs/browser.toml b/browser/components/tabbrowser/test/browser/tabs/browser.toml
index 7fd4004b7f9b..ea2dc3994e66 100644
--- a/browser/components/tabbrowser/test/browser/tabs/browser.toml
+++ b/browser/components/tabbrowser/test/browser/tabs/browser.toml
@@ -321,6 +321,8 @@ support-files = ["tab_that_opens_dialog.html"]
 ["browser_restore_isAppTab.js"]
 run-if = ["crashreporter"] # test requires crashreporter due to 1536221
 
+["browser_scroll_size_determination.js"]
+
 ["browser_selectTabAtIndex.js"]
 
 ["browser_switch_by_scrolling.js"]
diff --git a/browser/components/tabbrowser/test/browser/tabs/browser_scroll_size_determination.js b/browser/components/tabbrowser/test/browser/tabs/browser_scroll_size_determination.js
new file mode 100644
index 000000000000..685256c8d7da
--- /dev/null
+++ b/browser/components/tabbrowser/test/browser/tabs/browser_scroll_size_determination.js
@@ -0,0 +1,96 @@
+/* Any copyright is dedicated to the Public Domain.
+   https://creativecommons.org/publicdomain/zero/1.0/ */
+
+"use strict";
+
+/**
+ * Check that when opening a new window with vertical tabs turned
+ * on/off, wheel events with DOM_DELTA_LINE deltaMode successfully
+ * scroll the tabstrip.
+ */
+async function scrolling_works(useVerticalTabs, uiDensity) {
+  info(`Testing UI density ${uiDensity}`);
+
+  await SpecialPowers.pushPrefEnv({
+    set: [
+      ["sidebar.revamp", useVerticalTabs],
+      ["sidebar.verticalTabs", useVerticalTabs],
+    ],
+  });
+
+  let win = await BrowserTestUtils.openNewBrowserWindow();
+
+  win.gUIDensity.update(win.gUIDensity[uiDensity]);
+
+  await BrowserTestUtils.overflowTabs(registerCleanupFunction, win, {
+    overflowAtStart: false,
+    overflowTabFactor: 3,
+  });
+
+  await TestUtils.waitForCondition(() => {
+    return Array.from(win.gBrowser.tabs).every(tab => tab._fullyOpen);
+  });
+
+  win.gBrowser.pinTab(win.gBrowser.tabs[0]);
+
+  let firstScrollableTab = win.gBrowser.tabs[1];
+
+  // Scroll back to start.
+  win.gBrowser.selectedTab = firstScrollableTab;
+  await TestUtils.waitForTick();
+  await win.promiseDocumentFlushed(() => {});
+
+  // Check we're scrolled so the first scrollable tab is at the top.
+  let { arrowScrollbox } = win.gBrowser.tabContainer;
+  let side = useVerticalTabs ? "top" : "left";
+  let boxStart = arrowScrollbox.getBoundingClientRect()[side];
+  let firstPoint = boxStart + 5;
+  Assert.equal(
+    gBrowser.tabs.indexOf(arrowScrollbox._elementFromPoint(firstPoint)),
+    gBrowser.tabs.indexOf(firstScrollableTab),
+    "First tab should be scrolled into view."
+  );
+
+  // Scroll.
+  EventUtils.synthesizeWheel(
+    arrowScrollbox,
+    10,
+    10,
+    {
+      wheel: true,
+      deltaY: 1,
+      deltaMode: WheelEvent.DOM_DELTA_LINE,
+    },
+    win
+  );
+
+  // Check that some other tab is scrolled into view.
+  try {
+    await TestUtils.waitForCondition(() => {
+      return arrowScrollbox._elementFromPoint(firstPoint) != firstScrollableTab;
+    });
+  } catch (ex) {
+    Assert.ok(false, `Failed to see scroll, error: ${ex}`);
+  }
+  Assert.notEqual(
+    win.gBrowser.tabs.indexOf(arrowScrollbox._elementFromPoint(firstPoint)),
+    win.gBrowser.tabs.indexOf(firstScrollableTab),
+    "First tab should be scrolled out of view."
+  );
+
+  await SpecialPowers.popPrefEnv();
+
+  await BrowserTestUtils.closeWindow(win);
+}
+
+add_task(async function test_vertical_scroll() {
+  for (let density of ["MODE_NORMAL", "MODE_COMPACT", "MODE_TOUCH"]) {
+    await scrolling_works(true, density);
+  }
+});
+
+add_task(async function test_horizontal_scroll() {
+  for (let density of ["MODE_NORMAL", "MODE_COMPACT", "MODE_TOUCH"]) {
+    await scrolling_works(false, density);
+  }
+});
diff --git a/testing/mochitest/BrowserTestUtils/BrowserTestUtils.sys.mjs b/testing/mochitest/BrowserTestUtils/BrowserTestUtils.sys.mjs
index 0ba7474ceffb..367929e1e12f 100644
--- a/testing/mochitest/BrowserTestUtils/BrowserTestUtils.sys.mjs
+++ b/testing/mochitest/BrowserTestUtils/BrowserTestUtils.sys.mjs
@@ -1928,8 +1928,11 @@ export var BrowserTestUtils = {
     if (!params.hasOwnProperty("overflowTabFactor")) {
       params.overflowTabFactor = 1.1;
     }
-    let index = params.overflowAtStart ? 0 : undefined;
     let { gBrowser } = win;
+    let overflowDirection = gBrowser.tabContainer.verticalMode
+      ? "height"
+      : "width";
+    let index = params.overflowAtStart ? 0 : undefined;
     let arrowScrollbox = gBrowser.tabContainer.arrowScrollbox;
     if (arrowScrollbox.hasAttribute("overflowing")) {
       return;
@@ -1949,12 +1952,12 @@ export var BrowserTestUtils = {
       arrowScrollbox.smoothScroll = originalSmoothScroll;
     });
 
-    let width = ele => ele.getBoundingClientRect().width;
-    let tabMinWidth = parseInt(
-      win.getComputedStyle(gBrowser.selectedTab).minWidth
-    );
+    let size = ele => ele.getBoundingClientRect()[overflowDirection];
+    let tabMinSize = gBrowser.tabContainer.verticalMode
+      ? size(gBrowser.selectedTab)
+      : parseInt(win.getComputedStyle(gBrowser.selectedTab).minWidth);
     let tabCountForOverflow = Math.ceil(
-      (width(arrowScrollbox) / tabMinWidth) * params.overflowTabFactor
+      (size(arrowScrollbox) / tabMinSize) * params.overflowTabFactor
     );
     while (gBrowser.tabs.length < tabCountForOverflow) {
       promises.push(