diff --git a/changelog.d/19379.bugfix b/changelog.d/19379.bugfix
new file mode 100644
index 0000000000..6de9543bcc
--- /dev/null
+++ b/changelog.d/19379.bugfix
@@ -0,0 +1 @@
+Fix `InFlightGauge` typing to allow upgrading to `prometheus_client` 0.24.
diff --git a/scripts-dev/mypy_synapse_plugin.py b/scripts-dev/mypy_synapse_plugin.py
index 24794a1925..7fe4d6cd86 100644
--- a/scripts-dev/mypy_synapse_plugin.py
+++ b/scripts-dev/mypy_synapse_plugin.py
@@ -133,6 +133,7 @@ prometheus_metric_fullname_to_label_arg_map: Mapping[str, ArgLocation | None] =
     "prometheus_client.metrics.Info": ArgLocation("labelnames", 2),
     "prometheus_client.metrics.Enum": ArgLocation("labelnames", 2),
     "synapse.metrics.LaterGauge": ArgLocation("labelnames", 2),
+    "synapse.metrics._InFlightGaugeRuntime": ArgLocation("labels", 2),
     "synapse.metrics.InFlightGauge": ArgLocation("labels", 2),
     "synapse.metrics.GaugeBucketCollector": ArgLocation("labelnames", 2),
     "prometheus_client.registry.Collector": None,
diff --git a/synapse/metrics/__init__.py b/synapse/metrics/__init__.py
index b5ad6581e1..ba4334e372 100644
--- a/synapse/metrics/__init__.py
+++ b/synapse/metrics/__init__.py
@@ -27,6 +27,8 @@ import platform
 import threading
 from importlib import metadata
 from typing import (
+    TYPE_CHECKING,
+    Any,
     Callable,
     Generic,
     Iterable,
@@ -262,8 +264,12 @@ shutdown.
 MetricsEntry = TypeVar("MetricsEntry")
 
 
-class InFlightGauge(Generic[MetricsEntry], Collector):
-    """Tracks number of things (e.g. requests, Measure blocks, etc) in flight
+class _InFlightGaugeRuntime(Collector):
+    """
+    Runtime class for InFlightGauge. Contains all actual logic.
+    Does not inherit from Generic to avoid method resolution order (MRO) conflicts.
+
+    Tracks number of things (e.g. requests, Measure blocks, etc) in flight
     at any given time.
 
     Each InFlightGauge will create a metric called `<name>_total` that counts
@@ -292,16 +298,20 @@ class InFlightGauge(Generic[MetricsEntry], Collector):
 
         # Create a class which have the sub_metrics values as attributes, which
         # default to 0 on initialization. Used to pass to registered callbacks.
-        self._metrics_class: type[MetricsEntry] = attr.make_class(
+        self._metrics_class = attr.make_class(
             "_MetricsEntry",
             attrs={x: attr.ib(default=0) for x in sub_metrics},
             slots=True,
         )
 
         # Counts number of in flight blocks for a given set of label values
-        self._registrations: dict[
-            tuple[str, ...], set[Callable[[MetricsEntry], None]]
-        ] = {}
+        # `Callable` should be of type `Callable[[MetricsEntry], None]`, but
+        # `MetricsEntry` has no meaning in this context without the higher level
+        # `InFlightGauge` typing information.
+        # Instead, the typing is enforced by having `_registrations` be private and all
+        # accessor functions have proper `Callable[[MetricsEntry], None]` type
+        # annotations.
+        self._registrations: dict[tuple[str, ...], set[Callable[[Any], None]]] = {}
 
         # Protects access to _registrations
         self._lock = threading.Lock()
@@ -398,6 +408,17 @@ class InFlightGauge(Generic[MetricsEntry], Collector):
             yield gauge
 
 
+if TYPE_CHECKING:
+
+    class InFlightGauge(_InFlightGaugeRuntime, Generic[MetricsEntry]):
+        """
+        Typing-only generic wrapper.
+        Provides InFlightGauge[T] support to type checkers.
+        """
+else:
+    InFlightGauge = _InFlightGaugeRuntime
+
+
 class GaugeHistogramMetricFamilyWithLabels(GaugeHistogramMetricFamily):
     """
     Custom version of `GaugeHistogramMetricFamily` from `prometheus_client` that allows
diff --git a/synapse/util/metrics.py b/synapse/util/metrics.py
index 3daba79124..5e86939e37 100644
--- a/synapse/util/metrics.py
+++ b/synapse/util/metrics.py
@@ -19,6 +19,13 @@
 #
 #
 
+# These imports are necessary for python <= 3.13 in order for the `InFlightGauge` type
+# annotations not to be evaluated at runtime.
+# Starting with python 3.14, annotations are lazily evaluated by default, which is the
+# behaviour we desire.
+# More info here: https://docs.python.org/3/reference/compound_stmts.html#annotations
+from __future__ import annotations
+
 import logging
 from functools import wraps
 from types import TracebackType
diff --git a/tests/metrics/test_metrics.py b/tests/metrics/test_metrics.py
index 084eba3a5a..174b165679 100644
--- a/tests/metrics/test_metrics.py
+++ b/tests/metrics/test_metrics.py
@@ -18,6 +18,14 @@
 # [This file includes modifications made by New Vector Limited]
 #
 #
+
+# These imports are necessary for python <= 3.13 in order for the `InFlightGauge` type
+# annotations not to be evaluated at runtime.
+# Starting with python 3.14, annotations are lazily evaluated by default, which is the
+# behaviour we desire.
+# More info here: https://docs.python.org/3/reference/compound_stmts.html#annotations
+from __future__ import annotations
+
 from typing import NoReturn, Protocol
 
 from prometheus_client.core import Sample