diff --git a/CHANGELOG.md b/CHANGELOG.md
index 17e977d32df..0e30c2c622b 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -8,6 +8,7 @@
 - Fixed a bug where it wasn’t possible to save nested entries via the `entries/save-entry` controller action. ([#15737](https://github.com/craftcms/cms/issues/15737))
 - Fixed a bug where hyperlinks in Link field inputs could wrap unnecessarily. ([#15738](https://github.com/craftcms/cms/issues/15738))
 - Fixed an error that occurred when running the `entrify/global-set` command. ([#15746](https://github.com/craftcms/cms/issues/15746))
+- Fixed a bug where users’ `username` values weren’t getting updated based on email address changes when `useEmailAsUsername` was enabled. ([#15758](https://github.com/craftcms/cms/issues/15758))
 
 ## 5.4.4 - 2024-09-14
 
diff --git a/src/elements/User.php b/src/elements/User.php
index a0839883f9c..2c4ea48e7a3 100644
--- a/src/elements/User.php
+++ b/src/elements/User.php
@@ -910,7 +910,7 @@ protected function defineRules(): array
 
         if (Craft::$app->getIsInstalled()) {
             $rules[] = [
-                ['username', 'email'],
+                ['email'],
                 UniqueValidator::class,
                 'targetClass' => UserRecord::class,
                 'caseInsensitive' => true,
@@ -918,6 +918,17 @@ protected function defineRules(): array
                 'when' => $treatAsActive,
             ];
 
+            if (!Craft::$app->getConfig()->getGeneral()->useEmailAsUsername) {
+                $rules[] = [
+                    ['username'],
+                    UniqueValidator::class,
+                    'targetClass' => UserRecord::class,
+                    'caseInsensitive' => true,
+                    'filter' => ['or', ['active' => true], ['pending' => true]],
+                    'when' => $treatAsActive,
+                ];
+            }
+
             $rules[] = [['unverifiedEmail'], 'validateUnverifiedEmail'];
         }
 
@@ -2289,6 +2300,10 @@ final public function beforeSave(bool $isNew): bool
             return false;
         }
 
+        if (Craft::$app->getConfig()->getGeneral()->useEmailAsUsername) {
+            $this->username = $this->email;
+        }
+
         return parent::beforeSave($isNew);
     }
 
diff --git a/tests/unit/services/UsersTest.php b/tests/unit/services/UsersTest.php
index 540d5cb7c4d..8f83903b0eb 100644
--- a/tests/unit/services/UsersTest.php
+++ b/tests/unit/services/UsersTest.php
@@ -120,6 +120,8 @@ public function testUserActivationEmailAsUsernameWithAnUnverifedEmail(): void
 
         self::assertSame(User::STATUS_ACTIVE, $user->getStatus());
         self::assertSame('jsmith@gmail.com', $user->username);
+
+        Craft::$app->getConfig()->getGeneral()->useEmailAsUsername = false;
     }
 
     /**
@@ -139,6 +141,8 @@ public function testUserActivationEmailAsUsernameWithNoUnverifedEmail(): void
 
         self::assertSame(User::STATUS_ACTIVE, $user->getStatus());
         self::assertSame('jsmith', $user->username);
+
+        Craft::$app->getConfig()->getGeneral()->useEmailAsUsername = false;
     }
 
     /**