diff --git a/pydantic_ai_slim/pydantic_ai/_agent_graph.py b/pydantic_ai_slim/pydantic_ai/_agent_graph.py
index e121ec475a..e81711e8e6 100644
--- a/pydantic_ai_slim/pydantic_ai/_agent_graph.py
+++ b/pydantic_ai_slim/pydantic_ai/_agent_graph.py
@@ -167,7 +167,7 @@ class UserPromptNode(AgentNode[DepsT, NodeRunEndT]):
     system_prompt_functions: list[_system_prompt.SystemPromptRunner[DepsT]]
     system_prompt_dynamic_functions: dict[str, _system_prompt.SystemPromptRunner[DepsT]]
 
-    async def run(
+    async def run(  # noqa: C901
         self, ctx: GraphRunContext[GraphAgentState, GraphAgentDeps[DepsT, NodeRunEndT]]
     ) -> ModelRequestNode[DepsT, NodeRunEndT] | CallToolsNode[DepsT, NodeRunEndT]:
         try:
@@ -186,15 +186,6 @@ async def run(
         # Use the `capture_run_messages` list as the message history so that new messages are added to it
         ctx.state.message_history = messages
 
-        run_context = build_run_context(ctx)
-
-        parts: list[_messages.ModelRequestPart] = []
-        if messages:
-            # Reevaluate any dynamic system prompt parts
-            await self._reevaluate_dynamic_prompts(messages, run_context)
-        else:
-            parts.extend(await self._sys_parts(run_context))
-
         if (tool_call_results := ctx.deps.tool_call_results) is not None:
             if messages and (last_message := messages[-1]) and isinstance(last_message, _messages.ModelRequest):
                 # If tool call results were provided, that means the previous run ended on deferred tool calls.
@@ -209,21 +200,52 @@ async def run(
             if not messages:
                 raise exceptions.UserError('Tool call results were provided, but the message history is empty.')
 
+        next_message: _messages.ModelRequest | None = None
+
         if messages and (last_message := messages[-1]):
             if isinstance(last_message, _messages.ModelRequest) and self.user_prompt is None:
                 # Drop last message from history and reuse its parts
                 messages.pop()
-                parts.extend(last_message.parts)
+                next_message = _messages.ModelRequest(parts=last_message.parts)
+
+                # Extract `UserPromptPart` content from the popped message and add to `ctx.deps.prompt`
+                user_prompt_parts = [part for part in last_message.parts if isinstance(part, _messages.UserPromptPart)]
+                if user_prompt_parts:
+                    if len(user_prompt_parts) == 1:
+                        ctx.deps.prompt = user_prompt_parts[0].content
+                    else:
+                        combined_content: list[_messages.UserContent] = []
+                        for part in user_prompt_parts:
+                            if isinstance(part.content, str):
+                                combined_content.append(part.content)
+                            else:
+                                combined_content.extend(part.content)
+                        ctx.deps.prompt = combined_content
             elif isinstance(last_message, _messages.ModelResponse):
                 call_tools_node = await self._handle_message_history_model_response(ctx, last_message)
                 if call_tools_node is not None:
                     return call_tools_node
 
-        if self.user_prompt is not None:
-            parts.append(_messages.UserPromptPart(self.user_prompt))
+        # Build the run context after `ctx.deps.prompt` has been updated
+        run_context = build_run_context(ctx)
+
+        parts: list[_messages.ModelRequestPart] = []
+        if messages:
+            await self._reevaluate_dynamic_prompts(messages, run_context)
+
+        if next_message:
+            await self._reevaluate_dynamic_prompts([next_message], run_context)
+        else:
+            parts: list[_messages.ModelRequestPart] = []
+            if not messages:
+                parts.extend(await self._sys_parts(run_context))
+
+            if self.user_prompt is not None:
+                parts.append(_messages.UserPromptPart(self.user_prompt))
+
+            next_message = _messages.ModelRequest(parts=parts)
 
-        instructions = await ctx.deps.get_instructions(run_context)
-        next_message = _messages.ModelRequest(parts, instructions=instructions)
+        next_message.instructions = await ctx.deps.get_instructions(run_context)
 
         return ModelRequestNode[DepsT, NodeRunEndT](request=next_message)
 
diff --git a/tests/test_agent.py b/tests/test_agent.py
index 261cdfaee1..6ee8a0225f 100644
--- a/tests/test_agent.py
+++ b/tests/test_agent.py
@@ -2003,28 +2003,53 @@ async def ret_a(x: str) -> str:
 
 
 def test_run_with_history_ending_on_model_request_and_no_user_prompt():
+    m = TestModel()
+    agent = Agent(m)
+
+    @agent.system_prompt(dynamic=True)
+    async def system_prompt(ctx: RunContext) -> str:
+        return f'System prompt: user prompt length = {len(ctx.prompt or [])}'
+
     messages: list[ModelMessage] = [
-        ModelRequest(parts=[UserPromptPart(content='Hello')], instructions='Original instructions'),
+        ModelRequest(
+            parts=[
+                SystemPromptPart(content='System prompt', dynamic_ref=system_prompt.__qualname__),
+                UserPromptPart(content=['Hello', ImageUrl('https://example.com/image.jpg')]),
+                UserPromptPart(content='How goes it?'),
+            ],
+            instructions='Original instructions',
+        ),
     ]
 
-    m = TestModel()
-    agent = Agent(m, instructions='New instructions')
+    @agent.instructions
+    async def instructions(ctx: RunContext) -> str:
+        assert ctx.prompt == ['Hello', ImageUrl('https://example.com/image.jpg'), 'How goes it?']
+        return 'New instructions'
 
     result = agent.run_sync(message_history=messages)
     assert result.all_messages() == snapshot(
         [
             ModelRequest(
                 parts=[
+                    SystemPromptPart(
+                        content='System prompt: user prompt length = 3',
+                        timestamp=IsDatetime(),
+                        dynamic_ref=IsStr(),
+                    ),
                     UserPromptPart(
-                        content='Hello',
+                        content=['Hello', ImageUrl(url='https://example.com/image.jpg', identifier='39cfc4')],
                         timestamp=IsDatetime(),
-                    )
+                    ),
+                    UserPromptPart(
+                        content='How goes it?',
+                        timestamp=IsDatetime(),
+                    ),
                 ],
                 instructions='New instructions',
             ),
             ModelResponse(
                 parts=[TextPart(content='success (no tool calls)')],
-                usage=RequestUsage(input_tokens=51, output_tokens=4),
+                usage=RequestUsage(input_tokens=61, output_tokens=4),
                 model_name='test',
                 timestamp=IsDatetime(),
             ),