diff --git a/browser/components/BrowserContentHandler.jsm b/browser/components/BrowserContentHandler.jsm
index e018d59536cc..74a44078fd99 100644
--- a/browser/components/BrowserContentHandler.jsm
+++ b/browser/components/BrowserContentHandler.jsm
@@ -231,20 +231,18 @@ function openBrowserWindow(
   forcePrivate = false
 ) {
   let chromeURL = AppConstants.BROWSER_CHROME_URL;
+  const isStartup =
+    cmdLine && cmdLine.state == Ci.nsICommandLine.STATE_INITIAL_LAUNCH;
 
   let args;
   if (!urlOrUrlList) {
     // Just pass in the defaultArgs directly. We'll use system principal on the other end.
-    args = [gBrowserContentHandler.defaultArgs];
+    args = [gBrowserContentHandler.getArgs(isStartup)];
   } else {
     let pService = Cc["@mozilla.org/toolkit/profile-service;1"].getService(
       Ci.nsIToolkitProfileService
     );
-    if (
-      cmdLine &&
-      cmdLine.state == Ci.nsICommandLine.STATE_INITIAL_LAUNCH &&
-      pService.createdAlternateProfile
-    ) {
+    if (isStartup && pService.createdAlternateProfile) {
       let url = getNewInstallPage();
       if (Array.isArray(urlOrUrlList)) {
         urlOrUrlList.unshift(url);
@@ -295,7 +293,7 @@ function openBrowserWindow(
     }
   }
 
-  if (cmdLine && cmdLine.state == Ci.nsICommandLine.STATE_INITIAL_LAUNCH) {
+  if (isStartup) {
     let win = Services.wm.getMostRecentWindow("navigator:blank");
     if (win) {
       // Remove the windowtype of our blank window so that we don't close it
@@ -603,6 +601,10 @@ nsBrowserContentHandler.prototype = {
   /* nsIBrowserHandler */
 
   get defaultArgs() {
+    return this.getArgs();
+  },
+
+  getArgs(isStartup = false) {
     var prefb = Services.prefs;
 
     if (!gFirstWindow) {
@@ -688,6 +690,24 @@ nsBrowserContentHandler.prototype = {
       overridePage = "";
     }
 
+    // Allow showing a one-time startup override if we're not showing one
+    const ONCE_PREF = "browser.startup.homepage_override.once";
+    if (isStartup && overridePage == "" && prefb.prefHasUserValue(ONCE_PREF)) {
+      try {
+        // Show if we haven't passed the expiration or there's no expiration
+        const { expire, url } = JSON.parse(
+          Services.urlFormatter.formatURLPref(ONCE_PREF)
+        );
+        if (!(Date.now() > expire) && typeof url == "string") {
+          overridePage = url;
+        }
+      } catch (ex) {
+        // Invalid json pref, so ignore (and clear below)
+      } finally {
+        prefb.clearUserPref(ONCE_PREF);
+      }
+    }
+
     if (!additionalPage) {
       additionalPage = LaterRun.getURL() || "";
     }
diff --git a/browser/components/tests/browser/browser.ini b/browser/components/tests/browser/browser.ini
index c583c5180053..037d56ee1248 100644
--- a/browser/components/tests/browser/browser.ini
+++ b/browser/components/tests/browser/browser.ini
@@ -7,4 +7,5 @@ reason = test depends on update channel
 [browser_default_bookmark_toolbar_visibility.js]
 [browser_initial_tab_remoteType.js]
 fail-if = fission
+[browser_startup_homepage.js]
 [browser_urlbar_matchBuckets_migration60.js]
diff --git a/browser/components/tests/browser/browser_bug538331.js b/browser/components/tests/browser/browser_bug538331.js
index 50007de34c5c..03fda70c6600 100644
--- a/browser/components/tests/browser/browser_bug538331.js
+++ b/browser/components/tests/browser/browser_bug538331.js
@@ -81,8 +81,10 @@ const BCH_TESTS = [
 
 add_task(async function test_bug538331() {
   // Reset the startup page pref since it may have been set by other tests
-  // and we will assume it is default.
-  Services.prefs.clearUserPref("browser.startup.page");
+  // and we will assume it is (non-test) default.
+  await SpecialPowers.pushPrefEnv({
+    clear: [["browser.startup.page"]],
+  });
 
   let originalMstone = Services.prefs.getCharPref(PREF_MSTONE);
 
diff --git a/browser/components/tests/browser/browser_startup_homepage.js b/browser/components/tests/browser/browser_startup_homepage.js
new file mode 100644
index 000000000000..9df9150a28f3
--- /dev/null
+++ b/browser/components/tests/browser/browser_startup_homepage.js
@@ -0,0 +1,87 @@
+/* Any copyright is dedicated to the Public Domain.
+ * http://creativecommons.org/publicdomain/zero/1.0/ */
+
+"use strict";
+
+async function checkArgs(message, expect, prefs = {}) {
+  info(`Setting prefs: ${JSON.stringify(prefs)}`);
+  await SpecialPowers.pushPrefEnv({
+    set: Object.entries(prefs).map(keyVal => {
+      if (typeof keyVal[1] == "object") {
+        keyVal[1] = JSON.stringify(keyVal[1]);
+      }
+      return keyVal;
+    }),
+  });
+
+  // Check the defaultArgs for startup behavior
+  Assert.equal(
+    Cc["@mozilla.org/browser/clh;1"]
+      .getService(Ci.nsIBrowserHandler)
+      .wrappedJSObject.getArgs(true),
+    expect,
+    message
+  );
+}
+
+add_task(async function test_once_expire() {
+  const url = "https://www.mozilla.org/";
+  await checkArgs("no expiration", url, {
+    "browser.startup.homepage_override.once": { url },
+  });
+
+  await checkArgs("expired", "about:blank", {
+    "browser.startup.homepage_override.once": { expire: 0, url },
+  });
+
+  await checkArgs("not expired", url, {
+    "browser.startup.homepage_override.once": { expire: Date.now() * 2, url },
+  });
+});
+
+add_task(async function test_once_invalid() {
+  await checkArgs("not json", "about:blank", {
+    "browser.startup.homepage_override.once": "https://not.json",
+  });
+
+  await checkArgs("not string", "about:blank", {
+    "browser.startup.homepage_override.once": { url: 5 },
+  });
+});
+
+add_task(async function test_once() {
+  await checkArgs("initial test prefs (no homepage)", "about:blank");
+
+  const url = "https://www.mozilla.org/";
+  await checkArgs("override once", url, {
+    "browser.startup.homepage_override.once": { url },
+  });
+
+  await checkArgs("once cleared", "about:blank");
+
+  await checkArgs("formatted", "https://www.mozilla.org/en-US", {
+    "browser.startup.homepage_override.once": {
+      url: "https://www.mozilla.org/%LOCALE%",
+    },
+  });
+
+  await checkArgs("use homepage", "about:home", {
+    "browser.startup.page": 1,
+  });
+
+  await checkArgs("once with homepage", `${url}|about:home`, {
+    "browser.startup.homepage_override.once": { url },
+  });
+
+  await checkArgs("once cleared again", "about:home");
+
+  await checkArgs("prefer major version override", `about:welcome|about:home`, {
+    "browser.startup.homepage_override.mstone": "1.0",
+    "browser.startup.homepage_override.once": { url },
+    "startup.homepage_override_url": "about:welcome",
+  });
+
+  await checkArgs("once after major", `${url}|about:home`);
+
+  await checkArgs("once cleared yet again", "about:home");
+});