diff --git a/Dockerfile b/Dockerfile
index fade2a24e8..5bdc626989 100644
--- a/Dockerfile
+++ b/Dockerfile
@@ -10,5 +10,21 @@ RUN yarn install
 COPY . .
 RUN yarn build
 
+# Remove the default config, replace it with a symlink to somewhere that will be updated at runtime
+RUN rm -f target/assets/config.json \
+    && ln -sf /tmp/config.json target/assets/config.json
+
 FROM --platform=${TARGETPLATFORM} docker.io/nginxinc/nginx-unprivileged:1.21-alpine
+
+# Copy the config template as well as the templating script
+COPY ./docker/config.json.tmpl /config.json.tmpl
+COPY ./docker/config-template.sh /docker-entrypoint.d/99-config-template.sh
+
+# Copy the built app from the first build stage
 COPY --from=builder /app/target /usr/share/nginx/html
+
+# Values from the default config that can be overridden at runtime
+ENV PUSH_APP_ID="io.element.hydrogen.web" \
+    PUSH_GATEWAY_URL="https://matrix.org" \
+    PUSH_APPLICATION_SERVER_KEY="BC-gpSdVHEXhvHSHS0AzzWrQoukv2BE7KzpoPO_FfPacqOo3l1pdqz7rSgmB04pZCWaHPz7XRe6fjLaC-WPDopM" \
+    DEFAULT_HOMESERVER="matrix.org"
diff --git a/docker/config-template.sh b/docker/config-template.sh
new file mode 100755
index 0000000000..f6cff00c1d
--- /dev/null
+++ b/docker/config-template.sh
@@ -0,0 +1,7 @@
+#!/bin/sh
+
+set -eux
+
+envsubst '$PUSH_APP_ID,$PUSH_GATEWAY_URL,$PUSH_APPLICATION_SERVER_KEY,$DEFAULT_HOMESERVER' \
+    < /config.json.tmpl \
+    > /tmp/config.json
diff --git a/docker/config.json.tmpl b/docker/config.json.tmpl
new file mode 100644
index 0000000000..94295c43dd
--- /dev/null
+++ b/docker/config.json.tmpl
@@ -0,0 +1,8 @@
+{
+    "push": {
+        "appId": "$PUSH_APP_ID",
+        "gatewayUrl": "$PUSH_GATEWAY_URL",
+        "applicationServerKey": "$PUSH_APPLICATION_SERVER_KEY"
+    },
+    "defaultHomeServer": "$DEFAULT_HOMESERVER"
+}