diff --git a/changes/11505.fix.md b/changes/11505.fix.md
new file mode 100644
index 00000000000..61cbd99c3e8
--- /dev/null
+++ b/changes/11505.fix.md
@@ -0,0 +1 @@
+Fix `ResourceSlot.to_humanized()` to fall back to a guessed unit per slot instead of raising on missing slot type entries, preventing 500 errors from clobbering user-facing 4xx responses during error formatting.
diff --git a/src/ai/backend/common/types.py b/src/ai/backend/common/types.py
index 695a3bbd0d7..2dedb80dc7c 100644
--- a/src/ai/backend/common/types.py
+++ b/src/ai/backend/common/types.py
@@ -1223,14 +1223,17 @@ def from_user_input(
         return cls(data)
 
     def to_humanized(self, slot_types: Mapping[str, Any]) -> Mapping[str, str]:
-        try:
-            return {
-                k: type(self)._humanize_value(Decimal(v), slot_types[k])
-                for k, v in self.data.items()
-                if v is not None
-            }
-        except KeyError as e:
-            raise ValueError(f"Unknown slot type: {e.args[0]!r}") from e
+        def _resolve_unit(key: str) -> Any:
+            try:
+                return slot_types[key]
+            except KeyError:
+                return type(self)._guess_slot_type(key)
+
+        return {
+            k: type(self)._humanize_value(Decimal(v), _resolve_unit(k))
+            for k, v in self.data.items()
+            if v is not None
+        }
 
     @classmethod
     def from_json(cls, obj: Mapping[str, Any]) -> ResourceSlot:
diff --git a/tests/unit/common/test_types.py b/tests/unit/common/test_types.py
index ca583d710d2..5affea474f6 100644
--- a/tests/unit/common/test_types.py
+++ b/tests/unit/common/test_types.py
@@ -257,6 +257,30 @@ def test_resource_slot_serialization() -> None:
     assert r2["b"] == Decimal(0)
 
 
+def test_resource_slot_to_humanized_falls_back_for_unknown_slot() -> None:
+    # Missing keys fall back to the guessed unit instead of raising.
+    r = ResourceSlot({
+        "cpu": "1",
+        "mem": str(Decimal(2 * (2**30))),
+        "cuda.device": "1",
+        "cuda.mem": str(Decimal(1 * (2**30))),
+    })
+    slot_types: dict[str, str] = {"cpu": "count", "mem": "bytes"}
+    humanized = r.to_humanized(slot_types)
+    assert humanized == {
+        "cpu": "1",
+        "mem": "2g",
+        "cuda.device": "1",
+        "cuda.mem": "1g",
+    }
+
+
+def test_resource_slot_to_humanized_with_empty_slot_types() -> None:
+    r = ResourceSlot({"cuda.device": "2", "cuda.mem": str(Decimal(2**30))})
+    humanized = r.to_humanized({})
+    assert humanized == {"cuda.device": "2", "cuda.mem": "1g"}
+
+
 def test_resource_slot_serialization_prevent_scientific_notation() -> None:
     r1 = ResourceSlot({"a": "2E+1", "b": "200"})
     assert r1.to_json()["a"] == "20"