diff --git a/src/JsonSchema/DefinitionNameFactory.php b/src/JsonSchema/DefinitionNameFactory.php
index f70f3a37a6f..2396f9424d5 100644
--- a/src/JsonSchema/DefinitionNameFactory.php
+++ b/src/JsonSchema/DefinitionNameFactory.php
@@ -44,9 +44,10 @@ public function create(string $className, string $format = 'json', ?string $inpu
         }
 
         if (null !== $inputOrOutputClass && $className !== $inputOrOutputClass) {
-            $parts = explode('\\', $inputOrOutputClass);
-            $shortName = end($parts);
-            $prefix .= self::GLUE.$shortName;
+            // Use createPrefixFromClass so DTOs with identical short names but different
+            // FQCNs (e.g. App\...\Input\ThingCreate and App\...\Output\ThingCreate) get
+            // disambiguated suffixes instead of overwriting each other in the schema map.
+            $prefix .= self::GLUE.$this->createPrefixFromClass($inputOrOutputClass);
         }
 
         // TODO: remove in 5.0
diff --git a/src/JsonSchema/Tests/DefinitionNameFactoryTest.php b/src/JsonSchema/Tests/DefinitionNameFactoryTest.php
index 6257c4da70b..b297b8fae9f 100644
--- a/src/JsonSchema/Tests/DefinitionNameFactoryTest.php
+++ b/src/JsonSchema/Tests/DefinitionNameFactoryTest.php
@@ -15,8 +15,11 @@
 
 use ApiPlatform\JsonSchema\DefinitionNameFactory;
 use ApiPlatform\JsonSchema\SchemaFactory;
+use ApiPlatform\JsonSchema\Tests\Fixtures\DefinitionNameFactory\InputOutputCollision\Input\ThingCreate as InputThingCreate;
+use ApiPlatform\JsonSchema\Tests\Fixtures\DefinitionNameFactory\InputOutputCollision\Output\ThingCreate as OutputThingCreate;
 use ApiPlatform\Metadata\Get;
 use ApiPlatform\Metadata\Operation;
+use ApiPlatform\Metadata\Post;
 use ApiPlatform\Tests\Fixtures\TestBundle\ApiResource\DtoOutput;
 use ApiPlatform\Tests\Fixtures\TestBundle\Entity\Dummy;
 use PHPUnit\Framework\Attributes\DataProvider;
@@ -146,6 +149,35 @@ public function testCreateDifferentPrefixesForClassesWithTheSameShortName(): voi
         );
     }
 
+    public function testCreateDistinctDefinitionNamesWhenInputAndOutputShareShortName(): void
+    {
+        $definitionNameFactory = new DefinitionNameFactory();
+
+        $operation = new Post(class: Dummy::class, shortName: 'Thing');
+
+        $inputName = $definitionNameFactory->create(
+            Dummy::class,
+            'jsonld',
+            InputThingCreate::class,
+            $operation,
+            ['schema_type' => \ApiPlatform\JsonSchema\Schema::TYPE_INPUT]
+        );
+
+        $outputName = $definitionNameFactory->create(
+            Dummy::class,
+            'jsonld',
+            OutputThingCreate::class,
+            $operation,
+            ['schema_type' => \ApiPlatform\JsonSchema\Schema::TYPE_OUTPUT]
+        );
+
+        self::assertNotSame(
+            $inputName,
+            $outputName,
+            'Input and Output DTO classes sharing the same short name must produce distinct definition names.'
+        );
+    }
+
     public function testCreateDifferentPrefixesForClassesWithTheSameOperationShortName(): void
     {
         $definitionNameFactory = new DefinitionNameFactory();
diff --git a/src/JsonSchema/Tests/Fixtures/DefinitionNameFactory/InputOutputCollision/Input/ThingCreate.php b/src/JsonSchema/Tests/Fixtures/DefinitionNameFactory/InputOutputCollision/Input/ThingCreate.php
new file mode 100644
index 00000000000..c0b771c904d
--- /dev/null
+++ b/src/JsonSchema/Tests/Fixtures/DefinitionNameFactory/InputOutputCollision/Input/ThingCreate.php
@@ -0,0 +1,18 @@
+<?php
+
+/*
+ * This file is part of the API Platform project.
+ *
+ * (c) Kévin Dunglas <dunglas@gmail.com>
+ *
+ * For the full copyright and license information, please view the LICENSE
+ * file that was distributed with this source code.
+ */
+
+declare(strict_types=1);
+
+namespace ApiPlatform\JsonSchema\Tests\Fixtures\DefinitionNameFactory\InputOutputCollision\Input;
+
+class ThingCreate
+{
+}
diff --git a/src/JsonSchema/Tests/Fixtures/DefinitionNameFactory/InputOutputCollision/Output/ThingCreate.php b/src/JsonSchema/Tests/Fixtures/DefinitionNameFactory/InputOutputCollision/Output/ThingCreate.php
new file mode 100644
index 00000000000..acebe21f36d
--- /dev/null
+++ b/src/JsonSchema/Tests/Fixtures/DefinitionNameFactory/InputOutputCollision/Output/ThingCreate.php
@@ -0,0 +1,18 @@
+<?php
+
+/*
+ * This file is part of the API Platform project.
+ *
+ * (c) Kévin Dunglas <dunglas@gmail.com>
+ *
+ * For the full copyright and license information, please view the LICENSE
+ * file that was distributed with this source code.
+ */
+
+declare(strict_types=1);
+
+namespace ApiPlatform\JsonSchema\Tests\Fixtures\DefinitionNameFactory\InputOutputCollision\Output;
+
+class ThingCreate
+{
+}