diff --git a/nix/modules/hive-gateway.nix b/nix/modules/hive-gateway.nix
index d38e05de..aeaf6e72 100644
--- a/nix/modules/hive-gateway.nix
+++ b/nix/modules/hive-gateway.nix
@@ -326,21 +326,48 @@ in
                   # (https://spec.matrix.org/v1.15/client-server-api/#getwell-knownmatrixclient).
                   # No-op until the operator turns matrix on; until then
                   # there's no homeserver to advertise.
-                  lib.optionalAttrs (matrixCfg.enable && hyperhiveDomain != null) {
-                    "= /.well-known/matrix/client" = {
-                      extraConfig = ''
-                        default_type application/json;
-                        add_header Access-Control-Allow-Origin *;
-                        return 200 '{"m.homeserver":{"base_url":"http://${hyperhiveDomain}:${toString matrixCfg.httpPort}"}}';
-                      '';
-                    };
-                    "= /.well-known/matrix/server" = {
-                      extraConfig = ''
-                        default_type application/json;
-                        return 200 '{"m.server":"${hyperhiveDomain}:${toString matrixCfg.httpPort}"}';
-                      '';
-                    };
-                  }
+                  lib.optionalAttrs (matrixCfg.enable && hyperhiveDomain != null) (
+                    let
+                      # `.well-known/matrix/{client,server}` advertise where
+                      # the actual matrix API lives. When `matrixCfg.gatewayHost`
+                      # is set (default `matrix.<hive-domain>`, #747), point
+                      # at the sub-domain — no port suffix when the gateway
+                      # is on the canonical port 80, transparent to clients
+                      # (mara on #749:9609 sub-domain verdict, "not user-
+                      # visible because the .well-known redirect routes
+                      # clients through automatically"). When `gatewayHost`
+                      # is unset (no hive-domain, or operator nulled it),
+                      # fall back to the direct `host:port` shape — clients
+                      # reach tuwunel without going through the gateway,
+                      # no sub-domain delegation.
+                      portSuffix = if cfg.port == 80 then "" else ":${toString cfg.port}";
+                      clientBaseUrl =
+                        if matrixCfg.gatewayHost != null then
+                          "http://${matrixCfg.gatewayHost}${portSuffix}"
+                        else
+                          "http://${hyperhiveDomain}:${toString matrixCfg.httpPort}";
+                      serverHostPort =
+                        if matrixCfg.gatewayHost != null then
+                          "${matrixCfg.gatewayHost}${portSuffix}"
+                        else
+                          "${hyperhiveDomain}:${toString matrixCfg.httpPort}";
+                    in
+                    {
+                      "= /.well-known/matrix/client" = {
+                        extraConfig = ''
+                          default_type application/json;
+                          add_header Access-Control-Allow-Origin *;
+                          return 200 '{"m.homeserver":{"base_url":"${clientBaseUrl}"}}';
+                        '';
+                      };
+                      "= /.well-known/matrix/server" = {
+                        extraConfig = ''
+                          default_type application/json;
+                          return 200 '{"m.server":"${serverHostPort}"}';
+                        '';
+                      };
+                    }
+                  )
                 //
                   # Per-agent UIs (#15 v0). One `/agent/<name>/`
                   # block per `<name>: <port>` entry in
@@ -442,6 +469,61 @@ in
                     '';
                   };
                 };
+              }
+              //
+              # Matrix homeserver vhost (#747, mara verdict on #749:9609 —
+              # sub-domain over sub-path for matrix; "not user-visible"
+              # because clients discover the sub-domain via the
+              # `.well-known/matrix/{client,server}` delegation served
+              # above on the bare hive-domain).
+              #
+              # `server { server_name = matrixCfg.gatewayHost; }` proxies
+              # `/_matrix/...` → `http://127.0.0.1:''${matrixCfg.httpPort}/_matrix/...`.
+              # Tuwunel listens on `:''${httpPort}` (default 8008); the
+              # gateway terminates on `:''${cfg.port}` (80) so external
+              # clients speak matrix over the canonical web port without
+              # operators having to open the tuwunel port through firewalls.
+              #
+              # `/` returns 404 — nothing else lives at the matrix vhost;
+              # the matrix client-server API is entirely under `/_matrix/`,
+              # and federation under `/_matrix/federation/...`.
+              #
+              # CORS `*` on the matrix vhost per the matrix spec —
+              # federation + client requests come from any origin.
+              #
+              # `client_max_body_size 50M` covers typical media uploads
+              # (matrix-spec media size cap default); operators with bigger
+              # uploads override via the matrix module's own cap when that
+              # lands.
+              #
+              # `proxy_read_timeout 1h` for long-poll `/sync`; the default
+              # 60s would abort `/sync?timeout=30000` legitimately when
+              # tuwunel's keepalive exceeds that.
+              lib.optionalAttrs (matrixCfg.enable && matrixCfg.gatewayHost != null) {
+                "${matrixCfg.gatewayHost}" = {
+                  listen = [
+                    {
+                      addr = "0.0.0.0";
+                      port = cfg.port;
+                    }
+                  ];
+                  locations = {
+                    "/_matrix/" = {
+                      proxyPass = "http://127.0.0.1:${toString matrixCfg.httpPort}";
+                      proxyWebsockets = true;
+                      extraConfig = ''
+                        proxy_buffering off;
+                        client_max_body_size 50M;
+                        proxy_read_timeout 1h;
+                        proxy_send_timeout 1h;
+                        add_header Access-Control-Allow-Origin *;
+                      '';
+                    };
+                    "/" = {
+                      return = "404";
+                    };
+                  };
+                };
               };
           };
         };
@@ -452,16 +534,16 @@ in
     };
 
     # `/etc/hosts` entries for local dev: the bare hive domain plus
-    # any sub-domain modules (forge, matrix-via-#751) that are on.
-    # All map to `127.0.0.1` since the gateway shares host netns.
-    # Operators with real DNS leave `localHostsEntry = false`; this
-    # is the dev-loop shortcut for `http://<hive-domain>/` +
-    # `http://forge.<hive-domain>/` resolving locally.
+    # any sub-domain modules (forge via #749/#754, matrix via #747)
+    # that are on. All map to `127.0.0.1` since the gateway shares
+    # host netns. Operators with real DNS leave `localHostsEntry =
+    # false`; this is the dev-loop shortcut for `http://<hive-domain>/`
+    # + `http://forge.<hive-domain>/` + `http://matrix.<hive-domain>/`
+    # resolving locally.
     #
-    # Forge's `cfg.domain` may equal `hyperhiveDomain` (e.g. operator
-    # set `forge.domain = "darkest.space"` matching the hive domain)
-    # — `lib.unique` collapses the duplicate so `/etc/hosts` doesn't
-    # carry the same entry twice.
+    # `lib.unique` collapses any duplicate (e.g. if forge.domain
+    # happens to equal hyperhiveDomain or matrixCfg.gatewayHost) so
+    # `/etc/hosts` doesn't carry the same entry twice.
     networking.hosts = lib.mkIf (cfg.localHostsEntry && hyperhiveDomain != null) {
       "127.0.0.1" = lib.unique (
         [ hyperhiveDomain ]
@@ -469,6 +551,7 @@ in
           (config.services.hyperhive.forge.enable or false)
           && (config.services.hyperhive.forge.behindGateway or false)
         ) config.services.hyperhive.forge.domain
+        ++ lib.optional (matrixCfg.enable && matrixCfg.gatewayHost != null) matrixCfg.gatewayHost
       );
     };
   };
diff --git a/nix/modules/hive-matrix.nix b/nix/modules/hive-matrix.nix
index 907312aa..0b3b612f 100644
--- a/nix/modules/hive-matrix.nix
+++ b/nix/modules/hive-matrix.nix
@@ -252,6 +252,50 @@ in
       '';
     };
 
+    gatewayHost = lib.mkOption {
+      type = lib.types.nullOr lib.types.str;
+      default = if hyperhiveDomain != null then "matrix.${hyperhiveDomain}" else null;
+      defaultText = lib.literalExpression ''
+        if services.hyperhive.domain != null then
+          "matrix.''${services.hyperhive.domain}"
+        else
+          null
+      '';
+      example = "matrix.example.com";
+      description = ''
+        Public hostname for the matrix homeserver behind the
+        hive-gateway nginx (#747, mara verdict on #749:9609 — sub-domain
+        over sub-path for matrix, but **not user-visible** because the
+        `.well-known/matrix/{client,server}` redirect routes clients
+        through automatically).
+
+        When set + gateway is on, the gateway adds a `server { server_name
+        = gatewayHost; }` block that proxies `/_matrix/...` →
+        `http://127.0.0.1:''${httpPort}/_matrix/...`. The
+        `.well-known/matrix/{client,server}` endpoints (served by the
+        gateway at the bare hive-domain) then point at
+        `http(s)://''${gatewayHost}/` — matrix clients automatically
+        discover + follow that delegation.
+
+        Defaults to `matrix.''${services.hyperhive.domain}` when the
+        hive-domain is set (idiomatic matrix-spec shape — `matrix`
+        labelled under the hive's bare server_name domain). Defaults to
+        `null` when the hive-domain is unset (gateway vhost not added;
+        clients reach tuwunel directly on `httpPort`).
+
+        Set to a full hostname (`matrix.example.com`,
+        `homeserver.internal.lan`) for a bespoke vhost shape. Set to
+        `null` to disable the gateway vhost entirely (tuwunel stays
+        direct on `httpPort`).
+
+        **server_name vs gatewayHost**: `serverName` is the matrix
+        identifier domain embedded in user/room IDs irrevocably (per
+        #660 default = bare hive-domain). `gatewayHost` is just where
+        the API listens behind nginx. The two are different — see the
+        matrix-spec server-discovery flow.
+      '';
+    };
+
     openFirewall = lib.mkOption {
       type = lib.types.bool;
       default = false;