diff --git a/src/resources/formats/html/templates/quarto-html-before-body.ejs b/src/resources/formats/html/templates/quarto-html-before-body.ejs
index a81090e2bfa..931ff8f1db5 100644
--- a/src/resources/formats/html/templates/quarto-html-before-body.ejs
+++ b/src/resources/formats/html/templates/quarto-html-before-body.ejs
@@ -191,11 +191,12 @@
 
     <% if (respectUserColorScheme) { %>
     queryPrefersDark.addEventListener("change", e => {
-      if(window.localStorage.getItem("quarto-color-scheme") !== null)
-        return;
-      const alternate = e.matches
+      const alternate = e.matches;
+      if (window.localStorage.getItem("quarto-color-scheme") !== null) {
+        window.localStorage.removeItem("quarto-color-scheme");
+      }
       toggleColorMode(alternate);
-      localAlternateSentinel = e.matches ? 'alternate' : 'default'; // this is used alongside local storage!
+      localAlternateSentinel = alternate ? 'alternate' : 'default';
       toggleGiscusIfUsed(alternate, darkModeDefault);
     });
     <% } %>
diff --git a/tests/integration/playwright/tests/html-dark-mode-defaultdark.spec.ts b/tests/integration/playwright/tests/html-dark-mode-defaultdark.spec.ts
index a21c808674f..6796b42a2f9 100644
--- a/tests/integration/playwright/tests/html-dark-mode-defaultdark.spec.ts
+++ b/tests/integration/playwright/tests/html-dark-mode-defaultdark.spec.ts
@@ -89,7 +89,7 @@ test('Project specifies dark and light brands, dynamic respect-user-color-scheme
 });
 
 
-test('Project specifies dark and light brands, do not respect-user-color-scheme after toggling', async ({ page }) => {
+test('Project specifies dark and light brands, manual override expires on system theme change', async ({ page }) => {
   await page.goto('./html/dark-brand/project-dark/simple-respect-color-scheme.html');
   const locatr = await page.locator('body').first();
   await expect(locatr).toHaveClass(`fullcontent quarto-dark`);
@@ -100,8 +100,10 @@ test('Project specifies dark and light brands, do not respect-user-color-scheme
   await check_backgrounds(page, 'quarto-light', blue, red);
   await check_toggle(page, true);
 
+  // After the system theme changes, the manual override expires
+  // and the page follows the system again
   await page.emulateMedia({ colorScheme: 'light' });
-  await expect(locatr).toHaveClass(`fullcontent quarto-dark`);
-  await expect(locatr).toHaveCSS('background-color', red);
-  await check_toggle(page, true);
+  await expect(locatr).toHaveClass(`fullcontent quarto-light`);
+  await expect(locatr).toHaveCSS('background-color', blue);
+  await check_toggle(page, false);
 });