diff --git a/changelog.d/3956.bugfix b/changelog.d/3956.bugfix
new file mode 100644
index 000000000..b0828c9fc
--- /dev/null
+++ b/changelog.d/3956.bugfix
@@ -0,0 +1 @@
+Fix exceptions from metrics handler
\ No newline at end of file
diff --git a/synapse/util/caches/__init__.py b/synapse/util/caches/__init__.py
index 7b065b195..f37d5bec0 100644
--- a/synapse/util/caches/__init__.py
+++ b/synapse/util/caches/__init__.py
@@ -13,6 +13,7 @@
 # See the License for the specific language governing permissions and
 # limitations under the License.
 
+import logging
 import os
 
 import six
@@ -20,6 +21,8 @@ from six.moves import intern
 
 from prometheus_client.core import REGISTRY, Gauge, GaugeMetricFamily
 
+logger = logging.getLogger(__name__)
+
 CACHE_SIZE_FACTOR = float(os.environ.get("SYNAPSE_CACHE_FACTOR", 0.5))
 
 
@@ -76,16 +79,20 @@ def register_cache(cache_type, cache_name, cache):
             return []
 
         def collect(self):
-            if cache_type == "response_cache":
-                response_cache_size.labels(cache_name).set(len(cache))
-                response_cache_hits.labels(cache_name).set(self.hits)
-                response_cache_evicted.labels(cache_name).set(self.evicted_size)
-                response_cache_total.labels(cache_name).set(self.hits + self.misses)
-            else:
-                cache_size.labels(cache_name).set(len(cache))
-                cache_hits.labels(cache_name).set(self.hits)
-                cache_evicted.labels(cache_name).set(self.evicted_size)
-                cache_total.labels(cache_name).set(self.hits + self.misses)
+            try:
+                if cache_type == "response_cache":
+                    response_cache_size.labels(cache_name).set(len(cache))
+                    response_cache_hits.labels(cache_name).set(self.hits)
+                    response_cache_evicted.labels(cache_name).set(self.evicted_size)
+                    response_cache_total.labels(cache_name).set(self.hits + self.misses)
+                else:
+                    cache_size.labels(cache_name).set(len(cache))
+                    cache_hits.labels(cache_name).set(self.hits)
+                    cache_evicted.labels(cache_name).set(self.evicted_size)
+                    cache_total.labels(cache_name).set(self.hits + self.misses)
+            except Exception as e:
+                logger.warn("Error calculating metrics for %s: %s", cache_name, e)
+                raise
 
             yield GaugeMetricFamily("__unused", "")
 
diff --git a/synapse/util/caches/expiringcache.py b/synapse/util/caches/expiringcache.py
index 921a9c5b2..9af4ec4aa 100644
--- a/synapse/util/caches/expiringcache.py
+++ b/synapse/util/caches/expiringcache.py
@@ -16,6 +16,8 @@
 import logging
 from collections import OrderedDict
 
+from six import itervalues
+
 from synapse.metrics.background_process_metrics import run_as_background_process
 from synapse.util.caches import register_cache
 
@@ -54,8 +56,6 @@ class ExpiringCache(object):
 
         self.iterable = iterable
 
-        self._size_estimate = 0
-
         self.metrics = register_cache("expiring", cache_name, self)
 
         if not self._expiry_ms:
@@ -74,16 +74,11 @@ class ExpiringCache(object):
         now = self._clock.time_msec()
         self._cache[key] = _CacheEntry(now, value)
 
-        if self.iterable:
-            self._size_estimate += len(value)
-
         # Evict if there are now too many items
         while self._max_len and len(self) > self._max_len:
             _key, value = self._cache.popitem(last=False)
             if self.iterable:
-                removed_len = len(value.value)
-                self.metrics.inc_evictions(removed_len)
-                self._size_estimate -= removed_len
+                self.metrics.inc_evictions(len(value.value))
             else:
                 self.metrics.inc_evictions()
 
@@ -134,7 +129,9 @@ class ExpiringCache(object):
         for k in keys_to_delete:
             value = self._cache.pop(k)
             if self.iterable:
-                self._size_estimate -= len(value.value)
+                self.metrics.inc_evictions(len(value.value))
+            else:
+                self.metrics.inc_evictions()
 
         logger.debug(
             "[%s] _prune_cache before: %d, after len: %d",
@@ -143,7 +140,7 @@ class ExpiringCache(object):
 
     def __len__(self):
         if self.iterable:
-            return self._size_estimate
+            return sum(len(entry.value) for entry in itervalues(self._cache))
         else:
             return len(self._cache)