diff --git a/CHANGELOG b/CHANGELOG
index a3b240fff70..5e8a4aa1429 100644
--- a/CHANGELOG
+++ b/CHANGELOG
@@ -9,6 +9,7 @@
  * Add `TempestMarkdown` to use `tempest/markdown` as the `markdown_to_html` converter
  * Add the `include_only` function to render a template without giving it access to the current context
  * Add the `Twig\Sandbox\SandboxInterface` interface and `Twig\Sandbox\Sandbox` class to render untrusted templates through a dedicated, always-sandboxed environment crafted for it
+ * Reject `TemplateWrapper` instances created by another `Environment`
  * Add the `Twig\Extension\SandboxBridgeExtension` to render sandboxed templates from trusted templates with an explicit output escaping strategy
  * Extract the sandbox runtime enforcement into a new internal `Twig\Sandbox\SecurityChecker` class used by compiled templates and `CoreExtension`
  * Mark `SandboxExtension` as internal, use `Twig\Sandbox\Sandbox` instead
diff --git a/src/Environment.php b/src/Environment.php
index 05098f0b703..9f55e703c04 100644
--- a/src/Environment.php
+++ b/src/Environment.php
@@ -359,6 +359,8 @@ public function display($name, array $context = []): void
     public function load($name): TemplateWrapper
     {
         if ($name instanceof TemplateWrapper) {
+            $name->unwrap($this);
+
             return $name;
         }
         if ($name instanceof Template) {
@@ -503,7 +505,7 @@ public function resolveTemplate($names): TemplateWrapper
                 return new TemplateWrapper($this, $name);
             }
             if ($name instanceof TemplateWrapper) {
-                return $name;
+                return $this->load($name);
             }
 
             if (1 !== $count && !$this->getLoader()->exists($name)) {
diff --git a/src/Template.php b/src/Template.php
index aeca1467782..f7a58850a67 100644
--- a/src/Template.php
+++ b/src/Template.php
@@ -73,11 +73,15 @@ abstract public function getSourceContext(): Source;
      * This method is for internal use only and should never be called
      * directly.
      *
-     * @return self|TemplateWrapper|false The parent template or false if there is no parent
+     * @return self|false The parent template or false if there is no parent
      */
-    public function getParent(array $context): self|TemplateWrapper|false
+    public function getParent(array $context): self|false
     {
         if (null !== $this->parent) {
+            if ($this->parent instanceof TemplateWrapper) {
+                $this->parent = $this->load($this->parent, -1);
+            }
+
             return $this->parent;
         }
 
@@ -93,7 +97,10 @@ public function getParent(array $context): self|TemplateWrapper|false
             return false;
         }
 
-        if ($parent instanceof self || $parent instanceof TemplateWrapper) {
+        if ($parent instanceof TemplateWrapper) {
+            $parent = $this->load($parent, -1);
+        }
+        if ($parent instanceof self) {
             return $this->parents[$parent->getSourceContext()->getName()] = $parent;
         }
 
@@ -283,11 +290,11 @@ protected function load(string|TemplateWrapper|array $template, int $line, ?int
     {
         try {
             if (\is_array($template)) {
-                return $this->env->resolveTemplate($template)->unwrap();
+                return $this->env->resolveTemplate($template)->unwrap($this->env);
             }
 
             if ($template instanceof TemplateWrapper) {
-                return $template->unwrap();
+                return $template->unwrap($this->env);
             }
 
             if ($template === $this->getTemplateName()) {
diff --git a/src/TemplateWrapper.php b/src/TemplateWrapper.php
index afadc2b539c..a82b21059f2 100644
--- a/src/TemplateWrapper.php
+++ b/src/TemplateWrapper.php
@@ -11,6 +11,8 @@
 
 namespace Twig;
 
+use Twig\Error\RuntimeError;
+
 /**
  * Exposes a template to userland.
  *
@@ -96,11 +98,13 @@ public function getTemplateName(): string
 
     /**
      * @internal
-     *
-     * @return Template
      */
-    public function unwrap()
+    public function unwrap(Environment $env): Template
     {
+        if ($this->env !== $env) {
+            throw new RuntimeError(\sprintf('A "%s" can only be used with the "%s" that created it.', self::class, Environment::class));
+        }
+
         return $this->template;
     }
 }
diff --git a/tests/CallMacroTest.php b/tests/CallMacroTest.php
index 3b37daf91ec..f9e3f887e4c 100644
--- a/tests/CallMacroTest.php
+++ b/tests/CallMacroTest.php
@@ -235,6 +235,6 @@ private function load(array $templates): Template
     {
         $twig = new Environment(new ArrayLoader($templates));
 
-        return $twig->load('index')->unwrap();
+        return $twig->load('index')->unwrap($twig);
     }
 }
diff --git a/tests/EnvironmentTest.php b/tests/EnvironmentTest.php
index a4b0bf7714b..d311c2677b1 100644
--- a/tests/EnvironmentTest.php
+++ b/tests/EnvironmentTest.php
@@ -85,6 +85,17 @@ public function testAutoescapeOption(): void
         $this->assertEquals('foo\u003Cbr\/\u0020\u003E foo\u003Cbr\/\u0020\u003E', $twig->render('js', ['bar' => 'foo<br/ >']));
     }
 
+    public function testRejectsTemplateWrapperFromAnotherEnvironment(): void
+    {
+        $foreign = new Environment(new ArrayLoader(['index' => 'foreign']));
+        $twig = new Environment(new ArrayLoader());
+
+        $this->expectException(RuntimeError::class);
+        $this->expectExceptionMessage('can only be used with the "Twig\\Environment" that created it');
+
+        $twig->load($foreign->load('index'));
+    }
+
     public function escapingStrategyCallback($name)
     {
         return $name;
diff --git a/tests/Sandbox/SandboxTest.php b/tests/Sandbox/SandboxTest.php
index 220b072a8bb..19ee8817d80 100644
--- a/tests/Sandbox/SandboxTest.php
+++ b/tests/Sandbox/SandboxTest.php
@@ -11,8 +11,10 @@
 
 namespace Twig\Tests\Sandbox;
 
+use PHPUnit\Framework\Attributes\DataProvider;
 use PHPUnit\Framework\TestCase;
 use Twig\Environment;
+use Twig\Error\RuntimeError;
 use Twig\Extension\SandboxExtension;
 use Twig\Loader\ArrayLoader;
 use Twig\Markup;
@@ -228,6 +230,34 @@ public function testIncludedTemplatesAreSandboxed(): void
         $sandbox->render('index');
     }
 
+    /**
+     * @dataProvider provideForeignTemplateWrapperUsages
+     */
+    #[DataProvider('provideForeignTemplateWrapperUsages')]
+    public function testRejectsTemplateWrapperFromAnotherEnvironment(string $template, string $foreignTemplate, array $tags = [], array $functions = []): void
+    {
+        $foreign = self::env(['foreign' => $foreignTemplate]);
+        $sandbox = new Sandbox(self::env(['index' => $template]), self::strictPolicy(tags: $tags, functions: $functions));
+
+        $this->expectException(RuntimeError::class);
+        $this->expectExceptionMessage('can only be used with the "Twig\\Environment" that created it');
+
+        $sandbox->render('index', ['foreign' => $foreign->load('foreign')]);
+    }
+
+    public static function provideForeignTemplateWrapperUsages(): iterable
+    {
+        yield 'include tag' => ['{% include foreign %}', 'foreign content', ['include']];
+        yield 'include function' => ['{{ include(foreign) }}', 'foreign content', [], ['include']];
+        yield 'include function fallback' => ['{{ include(["missing", foreign]) }}', 'foreign content', [], ['include']];
+        yield 'include_only function' => ['{{ include_only(foreign) }}', 'foreign content', [], ['include_only']];
+        yield 'extends tag' => ['{% extends foreign %}', 'foreign content', ['extends']];
+        yield 'embed tag' => ['{% embed foreign %}{% endembed %}', 'foreign content', ['embed', 'extends']];
+        yield 'import tag' => ['{% import foreign as macros %}{{ macros.foo() }}', '{% macro foo() %}foreign content{% endmacro %}', ['import']];
+        yield 'from tag' => ['{% from foreign import foo %}{{ foo() }}', '{% macro foo() %}foreign content{% endmacro %}', ['from']];
+        yield 'block function' => ['{{ block("content", foreign) }}', '{% block content %}foreign content{% endblock %}', [], ['block']];
+    }
+
     public function testTheExtendsTagMustBeAllowed(): void
     {
         $templates = [
diff --git a/tests/TemplateWrapperTest.php b/tests/TemplateWrapperTest.php
index 475c22e6850..87513ed38a0 100644
--- a/tests/TemplateWrapperTest.php
+++ b/tests/TemplateWrapperTest.php
@@ -22,10 +22,24 @@
 
 use PHPUnit\Framework\TestCase;
 use Twig\Environment;
+use Twig\Error\RuntimeError;
 use Twig\Loader\ArrayLoader;
+use Twig\Template;
 
 class TemplateWrapperTest extends TestCase
 {
+    public function testUnwrapChecksTheEnvironment(): void
+    {
+        $twig = new Environment(new ArrayLoader(['index' => 'content']));
+        $wrapper = $twig->load('index');
+
+        $this->assertInstanceOf(Template::class, $wrapper->unwrap($twig));
+
+        $this->expectException(RuntimeError::class);
+        $this->expectExceptionMessage('can only be used with the "Twig\\Environment" that created it');
+        $wrapper->unwrap(new Environment(new ArrayLoader()));
+    }
+
     public function testHasGetBlocks(): void
     {
         $twig = new Environment(new ArrayLoader([