diff --git a/docs/gateway.md b/docs/gateway.md
index edc372fa..5f1d5e25 100644
--- a/docs/gateway.md
+++ b/docs/gateway.md
@@ -21,11 +21,13 @@ Per-agent UIs stay sub-path because they're hyperhive-internal and base-path-awa
 
 Operator points client at `<hive>`. Sequence:
 
-1. Client fetches `http://<hive>/.well-known/matrix/client` → `{"m.homeserver":{"base_url":"http://matrix.<hive>"}}` (no port suffix when gateway listens on 80).
+1. Client fetches `https://<hive>/.well-known/matrix/client` → `{"m.homeserver":{"base_url":"https://matrix.<hive>"}}` (no port suffix when gateway listens on 443). With `selfSignedTls = false` the scheme drops to http and the port suffix reflects the bare `port` instead.
 2. Client connects to `matrix.<hive>/_matrix/client/...`.
 3. Gateway routes `/_matrix/*` → tuwunel at `127.0.0.1:8008`.
 
-Federation peers fetch `.well-known/matrix/server` → `{"m.server":"matrix.<hive>"}` and connect to `matrix.<hive>:8448` per spec default. Gateway only listens on configured `port`; cross-hive federation needs either an SRV record (`_matrix._tcp.matrix.<hive>` → port 80) OR `matrix.openFirewall = true` so peers reach tuwunel's federation port directly. Hyperhive is mostly closed/internal, so this rarely bites.
+matrix-dart-sdk (FluffyChat etc.) hardcodes `https` for the well-known fetch regardless of input scheme, so the discovery endpoint MUST be https — see "Self-signed TLS" below for the cert generation that backs the default-on path.
+
+Federation peers fetch `.well-known/matrix/server` → `{"m.server":"matrix.<hive>"}` and connect to `matrix.<hive>:8448` per spec default. Gateway only listens on configured `port` (+ `httpsPort` when TLS on); cross-hive federation needs either an SRV record (`_matrix._tcp.matrix.<hive>` → port 80 / 443) OR `matrix.openFirewall = true` so peers reach tuwunel's federation port directly. Hyperhive is mostly closed/internal, so this rarely bites.
 
 ## SPA fallback (Accept-header pattern)
 
@@ -131,6 +133,22 @@ frontend-side derivation.
 
 Next-up tracked separately: #14 (container netns isolation), TLS (#594).
 
+## Self-signed TLS (`selfSignedTls`)
+
+On by default since #837. The gateway generates a self-signed RSA-4096 cert at first boot (10-year validity) and listens on `httpsPort` (default 443) on every vhost beside the plain-http `port` (default 80).
+
+**Why on by default**: matrix-dart-sdk (FluffyChat's SDK) hardcodes `https://<host>/.well-known/matrix/client` for homeserver discovery and refuses to fall back to plain http. Without TLS the browser client cannot bootstrap (#837). For headless agent traffic and operator dashboard reach plain http is fine, so the http listen stays in parallel — operators can keep using `http://<hive>/` from the dashboard if they don't care about the cert prompt.
+
+**Cert shape**: subject CN = bare hive domain; subjectAltName covers `<hive>` + wildcard `*.<hive>` so all current and future sub-domain vhosts (matrix, forge, ...) validate under the same cert. Stored at `/var/lib/hive-gateway/tls/{cert,key}.pem` inside the gateway container (`ephemeral = false`, so persisted across container restart).
+
+**Regeneration**: the generator unit (`hive-gateway-self-signed-cert.service`) is gated by `ConditionPathExists=!cert.pem`, so it's a one-shot. To rotate (e.g. cert leak, expiry approaching), delete `cert.pem` inside the gateway container and restart `nginx.service` — the generator runs as a `Before=` dependency. No automatic rotation; the cert is purely a workaround for the well-known fetch.
+
+**Production**: operators fronting hyperhive with a real reverse proxy (caddy + ACME, traefik + Let's Encrypt, etc.) set `selfSignedTls = false`. The proxy handles termination upstream, the gateway listens on `port` only.
+
+**Cert prompts**: browsers warn once per host on first visit. With the wildcard SAN, `https://<hive>/`, `https://matrix.<hive>/`, and `https://forge.<hive>/` are covered by the same cert, but the browser still prompts per origin (per-host security state). FluffyChat needs the user to accept both `matrix.<hive>` (the SPA itself) and `<hive>` (the well-known fetch endpoint).
+
+**`.well-known/matrix/{client,server}` scheme**: switches to `https` when `selfSignedTls` is on, so matrix-dart-sdk doesn't downgrade and tuwunel federation peers get a TLS-fronted base_url. The legacy `/matrix/*` 301 redirect also flips to https.
+
 ## Firewall posture (host-level)
 
 `hive-c0re.nix` opens the per-agent web-port range
@@ -141,6 +159,11 @@ Next-up tracked separately: #14 (container netns isolation), TLS (#594).
 firewall-open would defeat the single-front-door story (closes
 #621).
 
+`services.hyperhive.gateway.openFirewall = true` opens `port` plus
+`httpsPort` when `selfSignedTls = true` (default). Operators who
+flip `selfSignedTls = false` to front the gateway with a real
+TLS-terminating reverse proxy on the host get only `port` opened.
+
 Manager hashes into the same range since #753 (no more
 "manager pinned at 8000" special case), so one range opening covers
 every container.
diff --git a/nix/modules/hive-gateway.nix b/nix/modules/hive-gateway.nix
index df43b867..96fd876e 100644
--- a/nix/modules/hive-gateway.nix
+++ b/nix/modules/hive-gateway.nix
@@ -197,6 +197,46 @@ in
       '';
     };
 
+    selfSignedTls = lib.mkOption {
+      type = lib.types.bool;
+      default = true;
+      example = false;
+      description = ''
+        Generate a self-signed TLS cert at first gateway boot and
+        listen on `httpsPort` (default 443) with it on every vhost.
+        On by default because matrix-dart-sdk (the SDK behind
+        FluffyChat + several other Matrix clients) hardcodes
+        `https://<host>/.well-known/matrix/client` for homeserver
+        discovery and refuses to fall back to plain http — without
+        TLS the browser client just won't connect (#837).
+
+        Self-signed means browsers will show a "not secure" warning
+        on first visit; the operator clicks through once per
+        browser. For production deployments, set this to `false`
+        and front the gateway with a reverse proxy (caddy, traefik,
+        or nginx with ACME) that does proper TLS termination.
+
+        The cert is regenerated on demand if the file is missing
+        but never rotated automatically; delete
+        `/var/lib/hive-gateway/tls/cert.pem` inside the gateway
+        container to force a fresh one.
+
+        See `docs/gateway.md` ("Self-signed TLS").
+      '';
+    };
+
+    httpsPort = lib.mkOption {
+      type = lib.types.port;
+      default = 443;
+      example = 8443;
+      description = ''
+        TCP port for the TLS-terminated vhosts when `selfSignedTls`
+        is enabled. Default 443. Setting `selfSignedTls = false`
+        renders this option inert (the gateway listens on `port`
+        only).
+      '';
+    };
+
     agentPortsFile = lib.mkOption {
       type = lib.types.nullOr lib.types.path;
       default = "/var/lib/hyperhive/agent-ports.json";
@@ -311,8 +351,87 @@ in
       };
       config =
         { pkgs, ... }:
+        let
+          tlsDir = "/var/lib/hive-gateway/tls";
+          tlsCert = "${tlsDir}/cert.pem";
+          tlsKey = "${tlsDir}/key.pem";
+          # Listen addresses every vhost shares. Plain http on `cfg.port`
+          # always; `cfg.httpsPort` with TLS sits beside it when
+          # `cfg.selfSignedTls` is on. See `docs/gateway.md`
+          # ("Self-signed TLS") for the cert lifecycle.
+          vhostListen = [
+            {
+              addr = "0.0.0.0";
+              port = cfg.port;
+            }
+          ]
+          ++ lib.optional cfg.selfSignedTls {
+            addr = "0.0.0.0";
+            port = cfg.httpsPort;
+            ssl = true;
+          };
+          # nixos `services.nginx.virtualHosts.<name>` ssl attrs to mix
+          # into each vhost when self-signed TLS is on. `addSSL = true`
+          # is what gates `ssl_certificate` directive emission in the
+          # nixos nginx module (`hasSSL` checks addSSL / onlySSL /
+          # forceSSL). The actual ssl listen is the explicit entry
+          # with `ssl = true` in `vhostListen` — the nixos module's
+          # auto-listen-generation only kicks in when `listen` is
+          # empty, so the explicit listen wins and there's no
+          # duplicate-listen risk. Empty otherwise so the http-only
+          # path stays identical.
+          vhostTls = lib.optionalAttrs cfg.selfSignedTls {
+            addSSL = true;
+            sslCertificate = tlsCert;
+            sslCertificateKey = tlsKey;
+          };
+        in
         {
           system.stateVersion = "26.05";
+
+          # Generate a self-signed cert on first boot if missing. nginx
+          # waits on this (Before=) so we never start with a broken
+          # ssl_certificate path. Cert covers the bare hive domain plus
+          # `*.${hyperhiveDomain}` so the matrix + forge sub-domains
+          # are valid under the same cert. See `docs/gateway.md`
+          # ("Self-signed TLS").
+          systemd.services.hive-gateway-self-signed-cert = lib.mkIf cfg.selfSignedTls {
+            description = "Generate self-signed TLS cert for hive-gateway";
+            wantedBy = [ "multi-user.target" ];
+            before = [ "nginx.service" ];
+            unitConfig.ConditionPathExists = "!${tlsCert}";
+            serviceConfig = {
+              Type = "oneshot";
+              RemainAfterExit = true;
+              UMask = "0077";
+            };
+            path = [
+              pkgs.openssl
+              pkgs.coreutils
+            ];
+            script =
+              let
+                subjectCN = if hyperhiveDomain != null then hyperhiveDomain else "hyperhive.local";
+                # `subjectAltName` covers the bare hive + the canonical
+                # sub-domains. Includes a wildcard `*.${domain}` so any
+                # future sub-domain we mint (per-agent UI under a
+                # sub-domain, etc.) inherits the cert without a rebuild.
+                sanLines = lib.concatStringsSep "," (
+                  [ "DNS:${subjectCN}" ] ++ lib.optional (hyperhiveDomain != null) "DNS:*.${hyperhiveDomain}"
+                );
+              in
+              ''
+                mkdir -p ${tlsDir}
+                openssl req -x509 -newkey rsa:4096 -nodes -sha256 -days 3650 \
+                  -keyout ${tlsKey} \
+                  -out ${tlsCert} \
+                  -subj "/CN=${subjectCN}" \
+                  -addext "subjectAltName=${sanLines}"
+                chmod 0600 ${tlsKey}
+                chmod 0644 ${tlsCert}
+              '';
+          };
+
           services.nginx = {
             enable = true;
             recommendedProxySettings = true;
@@ -329,13 +448,8 @@ in
               }
             '';
             virtualHosts = {
-              "_" = {
-                listen = [
-                  {
-                    addr = "0.0.0.0";
-                    port = cfg.port;
-                  }
-                ];
+              "_" = vhostTls // {
+                listen = vhostListen;
                 locations =
                   # `<hive>/matrix/*` → 301 → `matrix.<hive>/$1`
                   # (fluffychat moved to sub-domain root in #772; this
@@ -344,8 +458,16 @@ in
                   # map.
                   lib.optionalAttrs (matrixCfg.enable && matrixCfg.gui.enable && matrixCfg.gatewayHost != null) (
                     let
-                      portSuffix = if cfg.port == 80 then "" else ":${toString cfg.port}";
-                      target = "http://${matrixCfg.gatewayHost}${portSuffix}";
+                      # Public-facing scheme + port-suffix. When self-signed TLS
+                      # is on, prefer https://<host> (matrix-spec compliance);
+                      # 443 elides the port. Otherwise fall back to the
+                      # plain-http listen with the bare port. See
+                      # `docs/gateway.md` ("Self-signed TLS").
+                      scheme = if cfg.selfSignedTls then "https" else "http";
+                      activePort = if cfg.selfSignedTls then cfg.httpsPort else cfg.port;
+                      defaultPort = if cfg.selfSignedTls then 443 else 80;
+                      portSuffix = if activePort == defaultPort then "" else ":${toString activePort}";
+                      target = "${scheme}://${matrixCfg.gatewayHost}${portSuffix}";
                     in
                     {
                       "/matrix/" = {
@@ -364,12 +486,15 @@ in
                     # client-bootstrap sequence.
                     lib.optionalAttrs (matrixCfg.enable && hyperhiveDomain != null) (
                       let
-                        portSuffix = if cfg.port == 80 then "" else ":${toString cfg.port}";
+                        scheme = if cfg.selfSignedTls then "https" else "http";
+                        activePort = if cfg.selfSignedTls then cfg.httpsPort else cfg.port;
+                        defaultPort = if cfg.selfSignedTls then 443 else 80;
+                        portSuffix = if activePort == defaultPort then "" else ":${toString activePort}";
                         clientBaseUrl =
                           if matrixCfg.gatewayHost != null then
-                            "http://${matrixCfg.gatewayHost}${portSuffix}"
+                            "${scheme}://${matrixCfg.gatewayHost}${portSuffix}"
                           else
-                            "http://${hyperhiveDomain}:${toString matrixCfg.httpPort}";
+                            "${scheme}://${hyperhiveDomain}:${toString matrixCfg.httpPort}";
                         serverHostPort =
                           if matrixCfg.gatewayHost != null then
                             "${matrixCfg.gatewayHost}${portSuffix}"
@@ -474,13 +599,8 @@ in
               # (multi-GB clones). SSH stays direct on `forge.sshPort`.
               # See `docs/gateway.md`.
               lib.optionalAttrs (forgeCfg.enable or false && forgeCfg.behindGateway or false) {
-                "${forgeCfg.domain}" = {
-                  listen = [
-                    {
-                      addr = "0.0.0.0";
-                      port = cfg.port;
-                    }
-                  ];
+                "${forgeCfg.domain}" = vhostTls // {
+                  listen = vhostListen;
                   locations."/" = {
                     proxyPass = "http://127.0.0.1:${toString forgeCfg.httpPort}/";
                     proxyWebsockets = true;
@@ -501,13 +621,8 @@ in
               # longer-prefix-wins puts `/_matrix/` ahead of `/`.
               # See `docs/gateway.md`.
               lib.optionalAttrs (matrixCfg.enable && matrixCfg.gatewayHost != null) {
-                "${matrixCfg.gatewayHost}" = {
-                  listen = [
-                    {
-                      addr = "0.0.0.0";
-                      port = cfg.port;
-                    }
-                  ];
+                "${matrixCfg.gatewayHost}" = vhostTls // {
+                  listen = vhostListen;
                   locations = {
                     "/_matrix/" = {
                       proxyPass = "http://127.0.0.1:${toString matrixCfg.httpPort}";
@@ -613,7 +728,7 @@ in
     };
 
     networking.firewall = lib.mkIf cfg.openFirewall {
-      allowedTCPPorts = [ cfg.port ];
+      allowedTCPPorts = [ cfg.port ] ++ lib.optional cfg.selfSignedTls cfg.httpsPort;
     };
 
     # `/etc/hosts` entries for local dev — bare hive domain + any