diff --git a/pydantic_ai_slim/pydantic_ai/ui/_adapter.py b/pydantic_ai_slim/pydantic_ai/ui/_adapter.py
index bb03147b71..58576941fe 100644
--- a/pydantic_ai_slim/pydantic_ai/ui/_adapter.py
+++ b/pydantic_ai_slim/pydantic_ai/ui/_adapter.py
@@ -2,7 +2,7 @@
 
 from abc import ABC, abstractmethod
 from collections.abc import AsyncIterator, Sequence
-from dataclasses import KW_ONLY, Field, dataclass, replace
+from dataclasses import KW_ONLY, Field, dataclass
 from functools import cached_property
 from http import HTTPStatus
 from typing import (
@@ -238,7 +238,7 @@ def run_stream_native(
             else:
                 state = raw_state
 
-            deps = replace(deps, state=state)
+            deps.state = state
         elif self.state:
             raise UserError(
                 f'State is provided but `deps` of type `{type(deps).__name__}` does not implement the `StateHandler` protocol: it needs to be a dataclass with a non-optional `state` field.'
diff --git a/pydantic_ai_slim/pydantic_ai/ui/ag_ui/app.py b/pydantic_ai_slim/pydantic_ai/ui/ag_ui/app.py
index 2d9cb434f0..1f0fbe5262 100644
--- a/pydantic_ai_slim/pydantic_ai/ui/ag_ui/app.py
+++ b/pydantic_ai_slim/pydantic_ai/ui/ag_ui/app.py
@@ -3,6 +3,7 @@
 from __future__ import annotations
 
 from collections.abc import Callable, Mapping, Sequence
+from dataclasses import replace
 from typing import Any, Generic
 
 from typing_extensions import Self
@@ -18,7 +19,7 @@
 from pydantic_ai.toolsets import AbstractToolset
 from pydantic_ai.usage import RunUsage, UsageLimits
 
-from .. import OnCompleteFunc
+from .. import OnCompleteFunc, StateHandler
 from ._adapter import AGUIAdapter
 
 try:
@@ -121,6 +122,12 @@ def __init__(
 
         async def run_agent(request: Request) -> Response:
             """Endpoint to run the agent with the provided input data."""
+            # `dispatch_request` will store the frontend state from the request on `deps.state` (if it implements the `StateHandler` protocol),
+            # so we need to copy the deps to avoid different requests mutating the same deps object.
+            nonlocal deps
+            if isinstance(deps, StateHandler):  # pragma: no branch
+                deps = replace(deps)
+
             return await AGUIAdapter[AgentDepsT, OutputDataT].dispatch_request(
                 request,
                 agent=agent,
diff --git a/tests/test_ag_ui.py b/tests/test_ag_ui.py
index 07d18bcfac..0ca9dcc3aa 100644
--- a/tests/test_ag_ui.py
+++ b/tests/test_ag_ui.py
@@ -1154,15 +1154,21 @@ async def store_state(
         ),
     ]
 
-    deps = StateDeps(StateInt(value=0))
+    seen_deps_states: list[int] = []
 
     for run_input in run_inputs:
         events = list[dict[str, Any]]()
-        async for event in run_ag_ui(agent, run_input, deps=deps):
+        deps = StateDeps(StateInt(value=0))
+
+        async def on_complete(result: AgentRunResult[Any]):
+            seen_deps_states.append(deps.state.value)
+
+        async for event in run_ag_ui(agent, run_input, deps=deps, on_complete=on_complete):
             events.append(json.loads(event.removeprefix('data: ')))
 
         assert events == simple_result()
     assert seen_states == snapshot([41, 0, 0, 42])
+    assert seen_deps_states == snapshot([42, 1, 1, 43])
 
 
 async def test_request_with_state_without_handler() -> None:
@@ -1275,8 +1281,10 @@ async def get_state(ctx: RunContext[StateDeps[StateInt]]) -> int:
 async def test_to_ag_ui() -> None:
     """Test the agent.to_ag_ui method."""
 
-    agent = Agent(model=FunctionModel(stream_function=simple_stream))
-    app = agent.to_ag_ui()
+    agent = Agent(model=FunctionModel(stream_function=simple_stream), deps_type=StateDeps[StateInt])
+
+    deps = StateDeps(StateInt(value=0))
+    app = agent.to_ag_ui(deps=deps)
     async with LifespanManager(app):
         transport = httpx.ASGITransport(app)
         async with httpx.AsyncClient(transport=transport) as client:
@@ -1286,6 +1294,7 @@ async def test_to_ag_ui() -> None:
                     id='msg_1',
                     content='Hello, world!',
                 ),
+                state=StateInt(value=42),
             )
             async with client.stream(
                 'POST',
@@ -1301,6 +1310,9 @@ async def test_to_ag_ui() -> None:
 
             assert events == simple_result()
 
+    # Verify the state was not mutated by the run
+    assert deps.state.value == 0
+
 
 async def test_callback_sync() -> None:
     """Test that sync callbacks work correctly."""