diff --git a/src/BlockChain.php b/src/BlockChain.php
index 64fa8652d..d9320ed01 100644
--- a/src/BlockChain.php
+++ b/src/BlockChain.php
@@ -58,12 +58,11 @@ final class BlockChain
                 throw new \TypeError(\sprintf('Block chain templates must be strings, "%s" or "%s" instances, "%s" given.', TemplateWrapper::class, self::class, get_debug_type($template)));
             }
 
-            $template = $template->unwrap();
             if (!$template->isOwnedBy($env)) {
                 throw new \LogicException('A block chain cannot contain templates from different Twig environments.');
             }
 
-            $this->templates[] = $template;
+            $this->templates[] = $template->unwrap($env);
         }
 
         if (!$this->templates) {
@@ -210,11 +209,7 @@ final class BlockChain
                 $parent = $template->getParent($context);
                 $fixed = $fixed && $template->hasFixedParent();
 
-                // a dynamic parent expression can evaluate to a template from another environment
-                $template = $parent instanceof TemplateWrapper ? $parent->unwrap() : $parent;
-                if (false !== $template && !$template->isOwnedBy($this->env)) {
-                    throw new \LogicException('A block chain cannot contain templates from different Twig environments.');
-                }
+                $template = $parent;
             } while (false !== $template);
         }
 
diff --git a/src/Environment.php b/src/Environment.php
index 2e0064353..0931c0da1 100644
--- a/src/Environment.php
+++ b/src/Environment.php
@@ -335,6 +335,8 @@ class Environment
     public function load(string|TemplateWrapper $name): TemplateWrapper
     {
         if ($name instanceof TemplateWrapper) {
+            $name->unwrap($this);
+
             return $name;
         }
 
@@ -471,7 +473,7 @@ class Environment
         $count = \count($names);
         foreach ($names as $name) {
             if ($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 24f78e96c..a25b05b41 100644
--- a/src/Template.php
+++ b/src/Template.php
@@ -80,9 +80,9 @@ abstract class Template
      * 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) {
             return $this->parent;
@@ -106,7 +106,10 @@ abstract class Template
             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;
         }
 
@@ -265,11 +268,11 @@ abstract class Template
     {
         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 c08fca5e3..ab1c414fd 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 +98,21 @@ final class TemplateWrapper
 
     /**
      * @internal
-     *
-     * @return Template
      */
-    public function unwrap()
+    public function isOwnedBy(Environment $env): bool
     {
+        return $this->env === $env && $this->template->isOwnedBy($env);
+    }
+
+    /**
+     * @internal
+     */
+    public function unwrap(Environment $env): Template
+    {
+        if (!$this->isOwnedBy($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/BlockChainTest.php b/tests/BlockChainTest.php
index f6258c424..59c076571 100644
--- a/tests/BlockChainTest.php
+++ b/tests/BlockChainTest.php
@@ -308,7 +308,7 @@ class BlockChainTest extends TestCase
     {
         $twig = new Environment(new ArrayLoader(['theme' => '']));
         $other = new Environment(new ArrayLoader(['theme' => '']));
-        $wrapper = new TemplateWrapper($twig, $other->load('theme')->unwrap());
+        $wrapper = new TemplateWrapper($twig, $other->load('theme')->unwrap($other));
 
         $this->expectException(\LogicException::class);
         $this->expectExceptionMessage('A block chain cannot contain templates from different Twig environments.');
@@ -322,8 +322,8 @@ class BlockChainTest extends TestCase
         $other = new Environment(new ArrayLoader(['parent' => '']));
         $chain = new BlockChain($twig, ['theme'], ['parent' => $other->load('parent')]);
 
-        $this->expectException(\LogicException::class);
-        $this->expectExceptionMessage('A block chain cannot contain templates from different Twig environments.');
+        $this->expectException(RuntimeError::class);
+        $this->expectExceptionMessage('A "Twig\TemplateWrapper" can only be used with the "Twig\Environment" that created it in "theme" at line 1.');
 
         $chain->getBlockNames();
     }
diff --git a/tests/CallMacroTest.php b/tests/CallMacroTest.php
index ec9b94b98..b1886f7c9 100644
--- a/tests/CallMacroTest.php
+++ b/tests/CallMacroTest.php
@@ -179,6 +179,6 @@ class CallMacroTest extends TestCase
     {
         $twig = new Environment(new ArrayLoader($templates));
 
-        return $twig->load('index')->unwrap();
+        return $twig->load('index')->unwrap($twig);
     }
 }
diff --git a/tests/EnvironmentTest.php b/tests/EnvironmentTest.php
index e44487df6..6ace44a51 100644
--- a/tests/EnvironmentTest.php
+++ b/tests/EnvironmentTest.php
@@ -81,6 +81,17 @@ class EnvironmentTest extends TestCase
         $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 5f8f88fdc..7c2ec3954 100644
--- a/tests/Sandbox/SandboxTest.php
+++ b/tests/Sandbox/SandboxTest.php
@@ -11,6 +11,7 @@
 
 namespace Twig\Tests\Sandbox;
 
+use PHPUnit\Framework\Attributes\DataProvider;
 use PHPUnit\Framework\TestCase;
 use Twig\Environment;
 use Twig\Error\RuntimeError;
@@ -221,6 +222,34 @@ class SandboxTest extends TestCase
         $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 970020343..36185b877 100644
--- a/tests/TemplateWrapperTest.php
+++ b/tests/TemplateWrapperTest.php
@@ -26,10 +26,23 @@ use Twig\Environment;
 use Twig\Error\LoaderError;
 use Twig\Error\RuntimeError;
 use Twig\Loader\ArrayLoader;
+use Twig\Template;
 use Twig\TwigFunction;
 
 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([