diff --git a/src/agents/tool.py b/src/agents/tool.py
index c8563e2e1b..cc38c082f8 100644
--- a/src/agents/tool.py
+++ b/src/agents/tool.py
@@ -552,6 +552,12 @@ def __agents_bind_function_tool__(
         return bound_invoker
 
     async def __call__(self, ctx: ToolContext[Any], input: str) -> Any:
+        if not isinstance(ctx, RunContextWrapper):
+            raise TypeError(
+                f"on_invoke_tool requires a ToolContext, got {type(ctx).__name__}. "
+                "Construct one with ToolContext(context=..., tool_name=..., "
+                "tool_call_id=..., tool_arguments=...) or invoke the tool through Runner."
+            )
         try:
             return await self._invoke_tool_impl(ctx, input)
         except Exception as e:
diff --git a/tests/test_function_tool.py b/tests/test_function_tool.py
index 60ae2558cc..476cf0d980 100644
--- a/tests/test_function_tool.py
+++ b/tests/test_function_tool.py
@@ -34,6 +34,7 @@
 )
 from agents.tool import default_tool_error_function
 from agents.tool_context import ToolContext
+from openai.types.responses import ResponseFunctionToolCall
 
 
 def argless_function() -> str:
@@ -1063,3 +1064,35 @@ def test_function_tool_timeout_error_function_must_be_callable() -> None:
             on_invoke_tool=_noop_on_invoke_tool,
             timeout_error_function=cast(Any, "not-callable"),
         )
+
+
+async def test_on_invoke_tool_rejects_non_tool_context() -> None:
+    """Calling on_invoke_tool with a non-context value should fail fast and clearly."""
+
+    @function_tool
+    def add(a: int, b: int) -> int:
+        """Add two numbers."""
+        return a + b
+
+    with pytest.raises(TypeError, match="on_invoke_tool requires a ToolContext"):
+        await add.on_invoke_tool(cast(Any, None), '{"a": 1, "b": 2}')
+
+    with pytest.raises(TypeError, match="on_invoke_tool requires a ToolContext"):
+        await add.on_invoke_tool(cast(Any, "not a context"), '{"a": 1, "b": 2}')
+
+    # A valid ToolContext should still work.
+    tool_call = ResponseFunctionToolCall(
+        type="function_call",
+        name="add",
+        call_id="call-add",
+        arguments='{"a": 1, "b": 2}',
+    )
+    tool_context = ToolContext(
+        context=None,
+        tool_name="add",
+        tool_call_id="call-add",
+        tool_arguments=tool_call.arguments,
+        tool_call=tool_call,
+    )
+    result = await add.on_invoke_tool(tool_context, tool_call.arguments)
+    assert result == 3