diff --git a/group_vars/matrix_servers b/group_vars/matrix_servers
index 88afb186d..11783fc68 100755
--- a/group_vars/matrix_servers
+++ b/group_vars/matrix_servers
@@ -18,6 +18,10 @@
 
 matrix_identity_server_url: "{{ ('https://' + matrix_server_fqn_matrix) if matrix_ma1sd_enabled else None }}"
 
+# If Synapse workers are enabled and matrix-nginx-proxy is disabled, certain APIs may not work over 'http://matrix-synapse:8008'.
+# This is because we explicitly disable them for the main Synapse process.
+matrix_homeserver_container_url: "{{ 'http://matrix-nginx-proxy:12080' if matrix_nginx_proxy_enabled else 'http://matrix-synapse:8008' }}"
+
 ######################################################################
 #
 # /matrix-base
@@ -283,7 +287,7 @@ matrix_mautrix_signal_systemd_required_services_list: |
 
 matrix_mautrix_signal_homeserver_domain: '{{ matrix_domain }}'
 
-matrix_mautrix_signal_homeserver_address: "{{ 'http://matrix-synapse:8008' if matrix_synapse_enabled else '' }}"
+matrix_mautrix_signal_homeserver_address: "{{ matrix_homeserver_container_url }}"
 
 matrix_mautrix_signal_homeserver_token: "{{ matrix_synapse_macaroon_secret_key | password_hash('sha512', 'si.hs.token') | to_uuid }}"
 
@@ -674,7 +678,7 @@ matrix_corporal_systemd_required_services_list: |
   }}
 
 # This goes to Synapse's vhost
-matrix_corporal_matrix_homeserver_api_endpoint: "http://matrix-nginx-proxy:12080"
+matrix_corporal_matrix_homeserver_api_endpoint: "{{ matrix_homeserver_container_url }}"
 
 matrix_corporal_matrix_auth_shared_secret: "{{ matrix_synapse_ext_password_provider_shared_secret_auth_shared_secret }}"
 
@@ -1388,7 +1392,7 @@ matrix_registration_riot_instance: "{{ ('https://' + matrix_server_fqn_element)
 
 matrix_registration_shared_secret: "{{ matrix_synapse_registration_shared_secret if matrix_synapse_enabled else '' }}"
 
-matrix_registration_server_location: "{{ 'http://matrix-synapse:8008' if matrix_synapse_enabled else '' }}"
+matrix_registration_server_location: "{{ matrix_homeserver_container_url }}"
 
 matrix_registration_api_validate_certs: "{{ false if matrix_ssl_retrieval_method == 'self-signed' else true }}"
 
diff --git a/roles/matrix-base/defaults/main.yml b/roles/matrix-base/defaults/main.yml
index d8285e1ca..02b5906dc 100644
--- a/roles/matrix-base/defaults/main.yml
+++ b/roles/matrix-base/defaults/main.yml
@@ -72,6 +72,11 @@ matrix_ntpd_service: "{{ 'ntpd' if ansible_os_family == 'RedHat' or ansible_dist
 
 matrix_homeserver_url: "https://{{ matrix_server_fqn_matrix }}"
 
+# Specifies where the homeserver is on the container network.
+# Where this is depends on whether there's a reverse-proxy in front of it, etc.
+# This likely gets overriden elsewhere.
+matrix_homeserver_container_url: "http://matrix-synapse:8008"
+
 matrix_identity_server_url: ~
 
 matrix_integration_manager_rest_url: ~
diff --git a/roles/matrix-bot-matrix-reminder-bot/defaults/main.yml b/roles/matrix-bot-matrix-reminder-bot/defaults/main.yml
index 29bc83073..c3deb2f27 100644
--- a/roles/matrix-bot-matrix-reminder-bot/defaults/main.yml
+++ b/roles/matrix-bot-matrix-reminder-bot/defaults/main.yml
@@ -58,7 +58,7 @@ matrix_bot_matrix_reminder_bot_matrix_user_id: '@{{ matrix_bot_matrix_reminder_b
 # The password that the bot uses to authenticate.
 matrix_bot_matrix_reminder_bot_matrix_user_password: ''
 
-matrix_bot_matrix_reminder_bot_matrix_homeserver_url: 'http://matrix-synapse:8008'
+matrix_bot_matrix_reminder_bot_matrix_homeserver_url: "{{ matrix_homeserver_container_url }}"
 
 # The timezone to use when creating reminders.
 # Examples: 'Europe/London', 'Etc/UTC'
diff --git a/roles/matrix-bridge-appservice-irc/defaults/main.yml b/roles/matrix-bridge-appservice-irc/defaults/main.yml
index ba4e1e1b2..e2c919261 100644
--- a/roles/matrix-bridge-appservice-irc/defaults/main.yml
+++ b/roles/matrix-bridge-appservice-irc/defaults/main.yml
@@ -14,7 +14,7 @@ matrix_appservice_irc_base_path: "{{ matrix_base_data_path }}/appservice-irc"
 matrix_appservice_irc_config_path: "{{ matrix_appservice_irc_base_path }}/config"
 matrix_appservice_irc_data_path: "{{ matrix_appservice_irc_base_path }}/data"
 
-matrix_appservice_irc_homeserver_url: 'http://matrix-synapse:8008'
+matrix_appservice_irc_homeserver_url: "{{ matrix_homeserver_container_url }}"
 matrix_appservice_irc_homeserver_media_url: 'https://{{ matrix_server_fqn_matrix }}'
 matrix_appservice_irc_homeserver_domain: '{{ matrix_domain }}'
 matrix_appservice_irc_homeserver_enablePresence: true
diff --git a/roles/matrix-bridge-mautrix-facebook/defaults/main.yml b/roles/matrix-bridge-mautrix-facebook/defaults/main.yml
index e99514e04..120c29602 100644
--- a/roles/matrix-bridge-mautrix-facebook/defaults/main.yml
+++ b/roles/matrix-bridge-mautrix-facebook/defaults/main.yml
@@ -16,7 +16,7 @@ matrix_mautrix_facebook_config_path: "{{ matrix_mautrix_facebook_base_path }}/co
 matrix_mautrix_facebook_data_path: "{{ matrix_mautrix_facebook_base_path }}/data"
 matrix_mautrix_facebook_docker_src_files_path: "{{ matrix_mautrix_facebook_base_path }}/docker-src"
 
-matrix_mautrix_facebook_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mautrix_facebook_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mautrix_facebook_homeserver_domain: '{{ matrix_domain }}'
 matrix_mautrix_facebook_appservice_address: 'http://matrix-mautrix-facebook:29319'
 
diff --git a/roles/matrix-bridge-mautrix-hangouts/defaults/main.yml b/roles/matrix-bridge-mautrix-hangouts/defaults/main.yml
index 8dfee030b..183c3ac73 100644
--- a/roles/matrix-bridge-mautrix-hangouts/defaults/main.yml
+++ b/roles/matrix-bridge-mautrix-hangouts/defaults/main.yml
@@ -18,7 +18,7 @@ matrix_mautrix_hangouts_docker_src_files_path: "{{ matrix_mautrix_hangouts_base_
 
 matrix_mautrix_hangouts_public_endpoint: '/mautrix-hangouts'
 
-matrix_mautrix_hangouts_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mautrix_hangouts_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mautrix_hangouts_homeserver_domain: '{{ matrix_domain }}'
 matrix_mautrix_hangouts_appservice_address: 'http://matrix-mautrix-hangouts:8080'
 
diff --git a/roles/matrix-bridge-mautrix-telegram/defaults/main.yml b/roles/matrix-bridge-mautrix-telegram/defaults/main.yml
index 7e072b5a5..5eab0c0b8 100644
--- a/roles/matrix-bridge-mautrix-telegram/defaults/main.yml
+++ b/roles/matrix-bridge-mautrix-telegram/defaults/main.yml
@@ -25,7 +25,7 @@ matrix_mautrix_telegram_bot_token: disabled
 # Example: /741a0483-ba17-4682-9900-30bd7269f1cc
 matrix_mautrix_telegram_public_endpoint: ''
 
-matrix_mautrix_telegram_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mautrix_telegram_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mautrix_telegram_homeserver_domain: '{{ matrix_domain }}'
 matrix_mautrix_telegram_appservice_address: 'http://matrix-mautrix-telegram:8080'
 matrix_mautrix_telegram_appservice_public_external: 'https://{{ matrix_server_fqn_matrix }}{{ matrix_mautrix_telegram_public_endpoint }}'
diff --git a/roles/matrix-bridge-mx-puppet-discord/defaults/main.yml b/roles/matrix-bridge-mx-puppet-discord/defaults/main.yml
index 97b203137..25f6ae06f 100644
--- a/roles/matrix-bridge-mx-puppet-discord/defaults/main.yml
+++ b/roles/matrix-bridge-mx-puppet-discord/defaults/main.yml
@@ -22,7 +22,7 @@ matrix_mx_puppet_discord_docker_src_files_path: "{{ matrix_mx_puppet_discord_bas
 
 matrix_mx_puppet_discord_appservice_port: "8432"
 
-matrix_mx_puppet_discord_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mx_puppet_discord_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mx_puppet_discord_homeserver_domain: '{{ matrix_domain }}'
 matrix_mx_puppet_discord_appservice_address: 'http://matrix-mx-puppet-discord:{{ matrix_mx_puppet_discord_appservice_port }}'
 
diff --git a/roles/matrix-bridge-mx-puppet-instagram/defaults/main.yml b/roles/matrix-bridge-mx-puppet-instagram/defaults/main.yml
index cd08c010a..4c9fbd989 100644
--- a/roles/matrix-bridge-mx-puppet-instagram/defaults/main.yml
+++ b/roles/matrix-bridge-mx-puppet-instagram/defaults/main.yml
@@ -16,7 +16,7 @@ matrix_mx_puppet_instagram_data_path: "{{ matrix_mx_puppet_instagram_base_path }
 matrix_mx_puppet_instagram_docker_src_files_path: "{{ matrix_mx_puppet_instagram_base_path }}/docker-src"
 
 matrix_mx_puppet_instagram_appservice_port: "8440"
-matrix_mx_puppet_instagram_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mx_puppet_instagram_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mx_puppet_instagram_homeserver_domain: '{{ matrix_domain }}'
 matrix_mx_puppet_instagram_appservice_address: 'http://matrix-mx-puppet-instagram:{{ matrix_mx_puppet_instagram_appservice_port }}'
 
diff --git a/roles/matrix-bridge-mx-puppet-skype/defaults/main.yml b/roles/matrix-bridge-mx-puppet-skype/defaults/main.yml
index 83cd3dc55..53c8e379b 100644
--- a/roles/matrix-bridge-mx-puppet-skype/defaults/main.yml
+++ b/roles/matrix-bridge-mx-puppet-skype/defaults/main.yml
@@ -17,7 +17,7 @@ matrix_mx_puppet_skype_docker_src_files_path: "{{ matrix_mx_puppet_skype_base_pa
 
 matrix_mx_puppet_skype_appservice_port: "8438"
 
-matrix_mx_puppet_skype_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mx_puppet_skype_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mx_puppet_skype_appservice_address: 'http://matrix-mx-puppet-skype:{{ matrix_mx_puppet_skype_appservice_port }}'
 
 # "@user:server.com" to allow specific user
diff --git a/roles/matrix-bridge-mx-puppet-slack/defaults/main.yml b/roles/matrix-bridge-mx-puppet-slack/defaults/main.yml
index 70b98ecee..b1fb7487f 100644
--- a/roles/matrix-bridge-mx-puppet-slack/defaults/main.yml
+++ b/roles/matrix-bridge-mx-puppet-slack/defaults/main.yml
@@ -22,7 +22,7 @@ matrix_mx_puppet_slack_docker_src_files_path: "{{ matrix_mx_puppet_slack_base_pa
 
 matrix_mx_puppet_slack_appservice_port: "8432"
 
-matrix_mx_puppet_slack_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mx_puppet_slack_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mx_puppet_slack_homeserver_domain: '{{ matrix_domain }}'
 matrix_mx_puppet_slack_appservice_address: 'http://matrix-mx-puppet-slack:{{ matrix_mx_puppet_slack_appservice_port }}'
 
diff --git a/roles/matrix-bridge-mx-puppet-steam/defaults/main.yml b/roles/matrix-bridge-mx-puppet-steam/defaults/main.yml
index 15fa889f0..c3ac977ee 100644
--- a/roles/matrix-bridge-mx-puppet-steam/defaults/main.yml
+++ b/roles/matrix-bridge-mx-puppet-steam/defaults/main.yml
@@ -22,7 +22,7 @@ matrix_mx_puppet_steam_docker_src_files_path: "{{ matrix_mx_puppet_steam_base_pa
 
 matrix_mx_puppet_steam_appservice_port: "8432"
 
-matrix_mx_puppet_steam_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mx_puppet_steam_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mx_puppet_steam_homeserver_domain: '{{ matrix_domain }}'
 matrix_mx_puppet_steam_appservice_address: 'http://matrix-mx-puppet-steam:{{ matrix_mx_puppet_steam_appservice_port }}'
 
diff --git a/roles/matrix-bridge-mx-puppet-twitter/defaults/main.yml b/roles/matrix-bridge-mx-puppet-twitter/defaults/main.yml
index 28639fdad..d8582e539 100644
--- a/roles/matrix-bridge-mx-puppet-twitter/defaults/main.yml
+++ b/roles/matrix-bridge-mx-puppet-twitter/defaults/main.yml
@@ -22,7 +22,7 @@ matrix_mx_puppet_twitter_docker_src_files_path: "{{ matrix_mx_puppet_twitter_bas
 
 matrix_mx_puppet_twitter_appservice_port: "8432"
 
-matrix_mx_puppet_twitter_homeserver_address: 'http://matrix-synapse:8008'
+matrix_mx_puppet_twitter_homeserver_address: "{{ matrix_homeserver_container_url }}"
 matrix_mx_puppet_twitter_homeserver_domain: '{{ matrix_domain }}'
 matrix_mx_puppet_twitter_appservice_address: 'http://matrix-mx-puppet-twitter:{{ matrix_mx_puppet_twitter_appservice_port }}'
 
diff --git a/roles/matrix-dimension/templates/config.yaml.j2 b/roles/matrix-dimension/templates/config.yaml.j2
index 200871e7e..39721d71f 100644
--- a/roles/matrix-dimension/templates/config.yaml.j2
+++ b/roles/matrix-dimension/templates/config.yaml.j2
@@ -13,7 +13,7 @@ homeserver:
 
   # The URL that Dimension, go-neb, and other services provisioned by Dimension should
   # use to access the homeserver with.
-  clientServerUrl: "http://matrix-synapse:8008"
+  clientServerUrl: "{{ matrix_homeserver_container_url }}"
 
   # The URL that Dimension should use when trying to communicate with federated APIs on
   # the homeserver. If not supplied or left empty Dimension will try to resolve the address