diff --git a/homeassistant/components/cloud/manifest.json b/homeassistant/components/cloud/manifest.json
index a21f09bf38ea..11e61ca17e7e 100644
--- a/homeassistant/components/cloud/manifest.json
+++ b/homeassistant/components/cloud/manifest.json
@@ -19,6 +19,6 @@
       "learn_more_url": "https://support.nabucasa.com/hc/en-us/articles/29718084245149-Speech-to-text-STT"
     }
   },
-  "requirements": ["hass-nabucasa==2.7.0", "openai==2.45.0"],
+  "requirements": ["hass-nabucasa==2.7.0", "openai==3.10.0"],
   "single_config_entry": true
 }
diff --git a/homeassistant/components/litellm/config_flow.py b/homeassistant/components/litellm/config_flow.py
index e22fbcce329d..177bf7e24ed7 100644
--- a/homeassistant/components/litellm/config_flow.py
+++ b/homeassistant/components/litellm/config_flow.py
@@ -1,7 +1,7 @@
 """Config flow for LiteLLM integration."""
 
 import logging
-from typing import Any, override
+from typing import Any, cast, override
 
 from openai import AsyncOpenAI, AuthenticationError, OpenAIError, PermissionDeniedError
 import voluptuous as vol
@@ -65,7 +65,8 @@ async def _get_models(hass: HomeAssistant, url: str, api_key: str | None) -> lis
     client = AsyncOpenAI(
         base_url=url,
         api_key=api_key or PLACEHOLDER_API_KEY,
-        http_client=get_async_client(hass),
+        # Legacy HTTPX clients are supported at runtime only.
+        http_client=cast(Any, get_async_client(hass)),
     )
     try:
         return [
diff --git a/homeassistant/components/litellm/coordinator.py b/homeassistant/components/litellm/coordinator.py
index ecd856bf6fd8..47cba3f72539 100644
--- a/homeassistant/components/litellm/coordinator.py
+++ b/homeassistant/components/litellm/coordinator.py
@@ -1,7 +1,7 @@
 """Coordinator for the LiteLLM integration."""
 
 from datetime import timedelta
-from typing import override
+from typing import Any, cast, override
 
 from openai import AsyncOpenAI, AuthenticationError, OpenAIError, PermissionDeniedError
 
@@ -40,7 +40,8 @@ class LiteLLMDataUpdateCoordinator(DataUpdateCoordinator[None]):
         self.client = AsyncOpenAI(
             base_url=config_entry.data[CONF_URL],
             api_key=config_entry.data.get(CONF_API_KEY) or PLACEHOLDER_API_KEY,
-            http_client=get_async_client(hass),
+            # Legacy HTTPX clients are supported at runtime only.
+            http_client=cast(Any, get_async_client(hass)),
         )
 
     @override
diff --git a/homeassistant/components/litellm/manifest.json b/homeassistant/components/litellm/manifest.json
index 595ec0710b38..5342871ba983 100644
--- a/homeassistant/components/litellm/manifest.json
+++ b/homeassistant/components/litellm/manifest.json
@@ -9,5 +9,5 @@
   "integration_type": "service",
   "iot_class": "cloud_polling",
   "quality_scale": "bronze",
-  "requirements": ["openai==2.45.0"]
+  "requirements": ["openai==3.10.0"]
 }
diff --git a/homeassistant/components/llama_cpp/api.py b/homeassistant/components/llama_cpp/api.py
index bf2c7bfa3959..5ee7f95014b6 100644
--- a/homeassistant/components/llama_cpp/api.py
+++ b/homeassistant/components/llama_cpp/api.py
@@ -62,7 +62,8 @@ async def async_create_client(
     client = openai.AsyncOpenAI(
         api_key=api_key,
         base_url=config_entry_data[CONF_BASE_URL],
-        http_client=get_async_client(hass),
+        # Legacy HTTPX clients are supported at runtime only.
+        http_client=cast(Any, get_async_client(hass)),
     )
     # Cache current platform data which gets added to each request
     # (caching done by library)
diff --git a/homeassistant/components/llama_cpp/manifest.json b/homeassistant/components/llama_cpp/manifest.json
index a610d9027208..b3599d7eeaf0 100644
--- a/homeassistant/components/llama_cpp/manifest.json
+++ b/homeassistant/components/llama_cpp/manifest.json
@@ -9,5 +9,5 @@
   "integration_type": "service",
   "iot_class": "local_polling",
   "quality_scale": "bronze",
-  "requirements": ["openai==2.45.0"]
+  "requirements": ["openai==3.10.0"]
 }
diff --git a/homeassistant/components/open_router/__init__.py b/homeassistant/components/open_router/__init__.py
index e25ab075383d..e09406740745 100644
--- a/homeassistant/components/open_router/__init__.py
+++ b/homeassistant/components/open_router/__init__.py
@@ -1,5 +1,7 @@
 """The OpenRouter integration."""
 
+from typing import Any, cast
+
 from openai import AsyncOpenAI, AuthenticationError, OpenAIError
 
 from homeassistant.config_entries import ConfigEntry
@@ -20,7 +22,8 @@ async def async_setup_entry(hass: HomeAssistant, entry: OpenRouterConfigEntry) -
     client = AsyncOpenAI(
         base_url="https://openrouter.ai/api/v1",
         api_key=entry.data[CONF_API_KEY],
-        http_client=get_async_client(hass),
+        # Legacy HTTPX clients are supported at runtime only.
+        http_client=cast(Any, get_async_client(hass)),
     )
 
     # Cache current platform data which gets added to each request
diff --git a/homeassistant/components/open_router/manifest.json b/homeassistant/components/open_router/manifest.json
index 8b835969cbe0..fa80c1fa7a19 100644
--- a/homeassistant/components/open_router/manifest.json
+++ b/homeassistant/components/open_router/manifest.json
@@ -9,5 +9,5 @@
   "integration_type": "service",
   "iot_class": "cloud_polling",
   "quality_scale": "bronze",
-  "requirements": ["openai==2.45.0", "python-open-router==0.4.0"]
+  "requirements": ["openai==3.10.0", "python-open-router==0.4.0"]
 }
diff --git a/homeassistant/components/openai_conversation/__init__.py b/homeassistant/components/openai_conversation/__init__.py
index 2ff1088ce1c9..67799727ed54 100644
--- a/homeassistant/components/openai_conversation/__init__.py
+++ b/homeassistant/components/openai_conversation/__init__.py
@@ -2,6 +2,7 @@
 
 from pathlib import Path
 from types import MappingProxyType
+from typing import Any, cast
 
 import openai
 from openai.types.images_response import ImagesResponse
@@ -282,7 +283,8 @@ async def async_setup_entry(hass: HomeAssistant, entry: OpenAIConfigEntry) -> bo
     """Set up OpenAI Conversation from a config entry."""
     client = openai.AsyncOpenAI(
         api_key=entry.data[CONF_API_KEY],
-        http_client=get_async_client(hass),
+        # Legacy HTTPX clients are supported at runtime only.
+        http_client=cast(Any, get_async_client(hass)),
     )
 
     # Cache current platform data which gets added to each request
@@ -290,7 +292,7 @@ async def async_setup_entry(hass: HomeAssistant, entry: OpenAIConfigEntry) -> bo
     _ = await hass.async_add_executor_job(client.platform_headers)
 
     try:
-        await hass.async_add_executor_job(client.with_options(timeout=10.0).models.list)
+        await client.models.list(timeout=10.0)
     except openai.AuthenticationError as err:
         raise ConfigEntryAuthFailed(err) from err
     except openai.OpenAIError as err:
diff --git a/homeassistant/components/openai_conversation/ai_task.py b/homeassistant/components/openai_conversation/ai_task.py
index e5ffa7516229..eb3caff7cec9 100644
--- a/homeassistant/components/openai_conversation/ai_task.py
+++ b/homeassistant/components/openai_conversation/ai_task.py
@@ -140,7 +140,7 @@ class OpenAITaskEntity(
         else:
             mime_type = "image/png"
 
-        if hasattr(image_call, "size") and (size := image_call.size):
+        if size := image_call.size:
             width, height = tuple(size.split("x"))
         else:
             width, height = None, None
diff --git a/homeassistant/components/openai_conversation/config_flow.py b/homeassistant/components/openai_conversation/config_flow.py
index 711d8e49db86..477769b96461 100644
--- a/homeassistant/components/openai_conversation/config_flow.py
+++ b/homeassistant/components/openai_conversation/config_flow.py
@@ -3,7 +3,7 @@
 from collections.abc import Mapping
 import json
 import logging
-from typing import Any, override
+from typing import Any, cast, override
 
 import openai
 from probatio import to_openapi
@@ -117,7 +117,9 @@ async def validate_input(hass: HomeAssistant, data: dict[str, Any]) -> None:
     Data has the keys from STEP_USER_DATA_SCHEMA with values provided by the user.
     """
     client = openai.AsyncOpenAI(
-        api_key=data[CONF_API_KEY], http_client=get_async_client(hass)
+        api_key=data[CONF_API_KEY],
+        # Legacy HTTPX clients are supported at runtime only.
+        http_client=cast(Any, get_async_client(hass)),
     )
     await client.models.list(timeout=10.0)
 
@@ -651,7 +653,7 @@ class OpenAISubentryFlowHandler(ConfigSubentryFlow):
         if zone_home is not None:
             client = openai.AsyncOpenAI(
                 api_key=self._get_entry().data[CONF_API_KEY],
-                http_client=get_async_client(self.hass),
+                http_client=cast(Any, get_async_client(self.hass)),
             )
             location_schema = vol.Schema(
                 {
diff --git a/homeassistant/components/openai_conversation/manifest.json b/homeassistant/components/openai_conversation/manifest.json
index 95fb8fc7d211..1af6e41921a0 100644
--- a/homeassistant/components/openai_conversation/manifest.json
+++ b/homeassistant/components/openai_conversation/manifest.json
@@ -9,5 +9,5 @@
   "integration_type": "service",
   "iot_class": "cloud_polling",
   "quality_scale": "bronze",
-  "requirements": ["openai==2.45.0"]
+  "requirements": ["openai==3.10.0"]
 }
diff --git a/homeassistant/components/ovhcloud_ai_endpoints/__init__.py b/homeassistant/components/ovhcloud_ai_endpoints/__init__.py
index 54f225060787..83667c6c367d 100644
--- a/homeassistant/components/ovhcloud_ai_endpoints/__init__.py
+++ b/homeassistant/components/ovhcloud_ai_endpoints/__init__.py
@@ -1,5 +1,7 @@
 """The OVHcloud AI Endpoints integration."""
 
+from typing import Any, cast
+
 from openai import (
     AsyncOpenAI,
     AuthenticationError,
@@ -27,7 +29,8 @@ def _create_client(hass: HomeAssistant, api_key: str) -> AsyncOpenAI:
     return AsyncOpenAI(
         base_url=BASE_URL,
         api_key=api_key,
-        http_client=get_async_client(hass),
+        # Legacy HTTPX clients are supported at runtime only.
+        http_client=cast(Any, get_async_client(hass)),
     )
 
 
diff --git a/homeassistant/components/ovhcloud_ai_endpoints/manifest.json b/homeassistant/components/ovhcloud_ai_endpoints/manifest.json
index 93feba804811..a1c56ee0592d 100644
--- a/homeassistant/components/ovhcloud_ai_endpoints/manifest.json
+++ b/homeassistant/components/ovhcloud_ai_endpoints/manifest.json
@@ -9,5 +9,5 @@
   "integration_type": "service",
   "iot_class": "cloud_polling",
   "quality_scale": "silver",
-  "requirements": ["openai==2.45.0"]
+  "requirements": ["openai==3.10.0"]
 }
diff --git a/homeassistant/package_constraints.txt b/homeassistant/package_constraints.txt
index edcb7114de95..17f13279796b 100644
--- a/homeassistant/package_constraints.txt
+++ b/homeassistant/package_constraints.txt
@@ -47,7 +47,7 @@ ifaddr==0.2.0
 Jinja2==3.1.6
 lru-dict==1.4.1
 mutagen==1.48.1
-openai==2.45.0
+openai==3.10.0
 orjson==3.11.9
 packaging>=23.1
 paho-mqtt==2.1.0
diff --git a/requirements_all.txt b/requirements_all.txt
index 57b5c23dc548..1b1321161254 100644
--- a/requirements_all.txt
+++ b/requirements_all.txt
@@ -1821,7 +1821,7 @@ open-meteo==0.3.2
 # homeassistant.components.open_router
 # homeassistant.components.openai_conversation
 # homeassistant.components.ovhcloud_ai_endpoints
-openai==2.45.0
+openai==3.10.0
 
 # homeassistant.components.openerz
 openerz-api==0.3.0
diff --git a/tests/components/openai_conversation/conftest.py b/tests/components/openai_conversation/conftest.py
index 22a18743394b..06a6b316765d 100644
--- a/tests/components/openai_conversation/conftest.py
+++ b/tests/components/openai_conversation/conftest.py
@@ -1,6 +1,6 @@
 """Tests helpers."""
 
-from collections.abc import Generator
+from collections.abc import AsyncGenerator, Generator
 from typing import Any
 from unittest.mock import AsyncMock, MagicMock, patch
 
@@ -122,13 +122,15 @@ async def mock_config_entry_with_reasoning_model(
 @pytest.fixture
 async def mock_init_component(
     hass: HomeAssistant, mock_config_entry: MockConfigEntry
-) -> None:
+) -> AsyncGenerator[None]:
     """Initialize integration."""
     with patch(
         "openai.resources.models.AsyncModels.list",
+        new_callable=AsyncMock,
     ):
         assert await async_setup_component(hass, DOMAIN, {})
         await hass.async_block_till_done()
+        yield
 
 
 @pytest.fixture(autouse=True)
diff --git a/tests/components/openai_conversation/test_init.py b/tests/components/openai_conversation/test_init.py
index 9a09697af7a9..06651c6d2d5c 100644
--- a/tests/components/openai_conversation/test_init.py
+++ b/tests/components/openai_conversation/test_init.py
@@ -277,12 +277,13 @@ async def test_init_error(
     hass: HomeAssistant,
     mock_config_entry: MockConfigEntry,
     caplog: pytest.LogCaptureFixture,
-    side_effect,
-    error,
+    side_effect: APIConnectionError | BadRequestError,
+    error: str,
 ) -> None:
     """Test initialization errors."""
     with patch(
         "openai.resources.models.AsyncModels.list",
+        new_callable=AsyncMock,
         side_effect=side_effect,
     ):
         assert await async_setup_component(hass, DOMAIN, {})
@@ -298,6 +299,7 @@ async def test_init_auth_error(
     """Test auth error during init errors."""
     with patch(
         "openai.resources.models.AsyncModels.list",
+        new_callable=AsyncMock,
         side_effect=AuthenticationError(
             response=httpx.Response(
                 status_code=500, request=httpx.Request(method="GET", url="test")