diff --git a/roles/custom/matrix-synapse-reverse-proxy-companion/defaults/main.yml b/roles/custom/matrix-synapse-reverse-proxy-companion/defaults/main.yml
index 3f19e3a2b..4a330e7a8 100644
--- a/roles/custom/matrix-synapse-reverse-proxy-companion/defaults/main.yml
+++ b/roles/custom/matrix-synapse-reverse-proxy-companion/defaults/main.yml
@@ -220,7 +220,9 @@ matrix_synapse_reverse_proxy_companion_synapse_stream_writer_receipts_stream_wor
 matrix_synapse_reverse_proxy_companion_synapse_stream_writer_presence_stream_worker_client_server_locations: []
 matrix_synapse_reverse_proxy_companion_synapse_media_repository_locations: []
 matrix_synapse_reverse_proxy_companion_synapse_user_dir_locations: []
-
+matrix_synapse_reverse_proxy_companion_client_server_main_override_locations_regex: ^/_matrix/client/(api/v1|r0|v3|unstable)/(account/3pid/|directory/list/room/|pushrules/|rooms/[^/]+/(forget|upgrade)|login/sso/redirect/|register)
+matrix_synapse_reverse_proxy_companion_client_server_sso_override_locations_regex: ^(/_matrix/client/(api/v1|r0|v3|unstable)/login/sso/redirect|/_synapse/client/(pick_username|(new_user_consent|oidc/callback|pick_idp|sso_register)$))
+matrix_synapse_reverse_proxy_companion_federation_override_locations_regex: ^/_matrix/federation/v1/openid/userinfo$
 
 # synapse content caching
 matrix_synapse_reverse_proxy_companion_synapse_cache_enabled: false
diff --git a/roles/custom/matrix-synapse-reverse-proxy-companion/templates/nginx/conf.d/matrix-synapse-reverse-proxy-companion.conf.j2 b/roles/custom/matrix-synapse-reverse-proxy-companion/templates/nginx/conf.d/matrix-synapse-reverse-proxy-companion.conf.j2
index 781b2edb3..81c9ced20 100644
--- a/roles/custom/matrix-synapse-reverse-proxy-companion/templates/nginx/conf.d/matrix-synapse-reverse-proxy-companion.conf.j2
+++ b/roles/custom/matrix-synapse-reverse-proxy-companion/templates/nginx/conf.d/matrix-synapse-reverse-proxy-companion.conf.j2
@@ -95,6 +95,36 @@ server {
 	gzip_types text/plain application/json;
 
 	{% if matrix_synapse_reverse_proxy_companion_synapse_workers_enabled %}
+		# Client-server overrides -- These locations must go to the main Synapse process
+		location ~ {{ matrix_synapse_reverse_proxy_companion_client_server_main_override_locations_regex }} {
+			{# FIXME: This block was copied from the main Synapse fallback below.  It would be better to have it in one place and avoid duplication. #}
+			{# Use the embedded DNS resolver in Docker containers to discover the service #}
+			resolver {{ matrix_synapse_reverse_proxy_companion_http_level_resolver }} valid=5s;
+			set $backend "{{ matrix_synapse_reverse_proxy_companion_client_api_addr }}";
+			proxy_pass http://$backend;
+
+			proxy_set_header Host $host;
+
+			client_body_buffer_size 25M;
+			client_max_body_size {{ matrix_synapse_reverse_proxy_companion_client_api_client_max_body_size_mb }}M;
+			proxy_max_temp_file_size 0;
+		}
+
+		# Client-server SSO overrides -- These locations must go to the main Synapse process
+		location ~ {{ matrix_synapse_reverse_proxy_companion_client_server_sso_override_locations_regex }} {
+			{# FIXME: This block was copied from the main Synapse fallback below.  It would be better to have it in one place and avoid duplication. #}
+			{# Use the embedded DNS resolver in Docker containers to discover the service #}
+			resolver {{ matrix_synapse_reverse_proxy_companion_http_level_resolver }} valid=5s;
+			set $backend "{{ matrix_synapse_reverse_proxy_companion_client_api_addr }}";
+			proxy_pass http://$backend;
+
+			proxy_set_header Host $host;
+
+			client_body_buffer_size 25M;
+			client_max_body_size {{ matrix_synapse_reverse_proxy_companion_client_api_client_max_body_size_mb }}M;
+			proxy_max_temp_file_size 0;
+		}
+
 		{# Workers redirects BEGIN #}
 
 		{% if room_workers | length > 0 %}
@@ -203,6 +233,21 @@ server {
 	gzip_types text/plain application/json;
 
 	{% if matrix_synapse_reverse_proxy_companion_synapse_workers_enabled %}
+		# Federation overrides -- These locations must go to the main Synapse process
+		location ~ {{ matrix_synapse_reverse_proxy_companion_federation_override_locations_regex }} {
+			{# FIXME: This block was copied from the fallback location below.  It would be better to have it in one place and avoid duplication. #}
+			{# Use the embedded DNS resolver in Docker containers to discover the service #}
+			resolver {{ matrix_synapse_reverse_proxy_companion_http_level_resolver }} valid=5s;
+			set $backend "{{ matrix_synapse_reverse_proxy_companion_federation_api_addr }}";
+			proxy_pass http://$backend;
+
+			proxy_set_header Host $host;
+
+			client_body_buffer_size 25M;
+			client_max_body_size {{ matrix_synapse_reverse_proxy_companion_federation_api_client_max_body_size_mb }}M;
+			proxy_max_temp_file_size 0;
+		}
+
 		{% if room_workers | length > 0 %}
 			# https://tcpipuk.github.io/synapse/deployment/workers.html
 			{{ render_locations_to_upstream(matrix_synapse_reverse_proxy_companion_synapse_room_worker_federation_locations, 'room_workers_upstream') }}