diff --git a/installer/templates/phx_single/config/dev.exs b/installer/templates/phx_single/config/dev.exs
index 95a5fa1fe4..482e8176a7 100644
--- a/installer/templates/phx_single/config/dev.exs
+++ b/installer/templates/phx_single/config/dev.exs
@@ -10,10 +10,10 @@ config :<%= @app_name %>, <%= @endpoint_module %>,<%= if @inside_docker_env? do
   # Bind to 0.0.0.0 to expose the server to the docker host machine.
   # This makes make the service accessible from any network interface.
   # Change to `ip: {127, 0, 0, 1}` to allow access only from the server machine.
-  http: [ip: {0, 0, 0, 0}, port: String.to_integer(System.get_env("PORT") || "4000")],<% else %>
+  http: [ip: {0, 0, 0, 0}],<% else %>
   # Binding to loopback ipv4 address prevents access from other machines.
   # Change to `ip: {0, 0, 0, 0}` to allow access from other machines.
-  http: [ip: {127, 0, 0, 1}, port: String.to_integer(System.get_env("PORT") || "4000")],<% end %>
+  http: [ip: {127, 0, 0, 1}],<% end %>
   check_origin: false,
   code_reloader: true,
   debug_errors: true,
diff --git a/installer/templates/phx_single/config/runtime.exs b/installer/templates/phx_single/config/runtime.exs
index 7f2d1d608d..675e0feb8c 100644
--- a/installer/templates/phx_single/config/runtime.exs
+++ b/installer/templates/phx_single/config/runtime.exs
@@ -20,6 +20,9 @@ if System.get_env("PHX_SERVER") do
   config :<%= @app_name %>, <%= @endpoint_module %>, server: true
 end
 
+config :<%= @app_name %>, <%= @endpoint_module %>,
+  http: [port: String.to_integer(System.get_env("PORT", "4000"))]
+
 if config_env() == :prod do
   # The secret key base is used to sign/encrypt cookies and other secrets.
   # A default value is used in config/dev.exs and config/test.exs but you
@@ -34,7 +37,6 @@ if config_env() == :prod do
       """
 
   host = System.get_env("PHX_HOST") || "example.com"
-  port = String.to_integer(System.get_env("PORT") || "4000")
 
   config :<%= @app_name %>, :dns_cluster_query, System.get_env("DNS_CLUSTER_QUERY")
 
@@ -45,8 +47,7 @@ if config_env() == :prod do
       # Set it to  {0, 0, 0, 0, 0, 0, 0, 1} for local network only access.
       # See the documentation on <%= @web_adapter_docs %>
       # for details about using IPv6 vs IPv4 and loopback vs public addresses.
-      ip: {0, 0, 0, 0, 0, 0, 0, 0},
-      port: port
+      ip: {0, 0, 0, 0, 0, 0, 0, 0}
     ],
     secret_key_base: secret_key_base
 
diff --git a/installer/templates/phx_umbrella/apps/app_name_web/config/dev.exs b/installer/templates/phx_umbrella/apps/app_name_web/config/dev.exs
index 8cecdd2bb0..6a044c4131 100644
--- a/installer/templates/phx_umbrella/apps/app_name_web/config/dev.exs
+++ b/installer/templates/phx_umbrella/apps/app_name_web/config/dev.exs
@@ -10,10 +10,10 @@ config :<%= @web_app_name %>, <%= @endpoint_module %>,<%= if @inside_docker_env?
   # Bind to 0.0.0.0 to expose the server to the docker host machine.
   # This makes make the service accessible from any network interface.
   # Change to `ip: {127, 0, 0, 1}` to allow access only from the server machine.
-  http: [ip: {0, 0, 0, 0}, port: String.to_integer(System.get_env("PORT") || "4000")],<% else %>
+  http: [ip: {0, 0, 0, 0}],<% else %>
   # Binding to loopback ipv4 address prevents access from other machines.
   # Change to `ip: {0, 0, 0, 0}` to allow access from other machines.
-  http: [ip: {127, 0, 0, 1}, port: String.to_integer(System.get_env("PORT") || "4000")],<% end %>
+  http: [ip: {127, 0, 0, 1}],<% end %>
   check_origin: false,
   code_reloader: true,
   debug_errors: true,
diff --git a/installer/templates/phx_umbrella/apps/app_name_web/config/runtime.exs b/installer/templates/phx_umbrella/apps/app_name_web/config/runtime.exs
index e32393f177..8b62c9db4c 100644
--- a/installer/templates/phx_umbrella/apps/app_name_web/config/runtime.exs
+++ b/installer/templates/phx_umbrella/apps/app_name_web/config/runtime.exs
@@ -14,8 +14,7 @@ config :<%= @web_app_name %>, <%= @endpoint_module %>,
   http: [
     # Enable IPv6 and bind on all interfaces.
     # Set it to  {0, 0, 0, 0, 0, 0, 0, 1} for local network only access.
-    ip: {0, 0, 0, 0, 0, 0, 0, 0},
-    port: String.to_integer(System.get_env("PORT") || "4000")
+    ip: {0, 0, 0, 0, 0, 0, 0, 0}
   ],
   secret_key_base: secret_key_base
 
diff --git a/installer/templates/phx_umbrella/config/runtime.exs b/installer/templates/phx_umbrella/config/runtime.exs
index 587a07f8a7..6e56791aa0 100644
--- a/installer/templates/phx_umbrella/config/runtime.exs
+++ b/installer/templates/phx_umbrella/config/runtime.exs
@@ -6,6 +6,10 @@ import Config
 # and secrets from environment variables or elsewhere. Do not define
 # any compile-time configuration in here, as it won't be applied.
 # The block below contains prod specific runtime configuration.
+
+config :<%= @app_name %>, <%= @endpoint_module %>,
+  http: [port: String.to_integer(System.get_env("PORT", "4000"))]
+
 if config_env() == :prod do
   config :<%= @app_name %>, :dns_cluster_query, System.get_env("DNS_CLUSTER_QUERY")
 end
diff --git a/installer/test/phx_new_test.exs b/installer/test/phx_new_test.exs
index c1c1166f62..7df19fce61 100644
--- a/installer/test/phx_new_test.exs
+++ b/installer/test/phx_new_test.exs
@@ -64,7 +64,12 @@ defmodule Mix.Tasks.Phx.NewTest do
         assert file =~ "config :logger, level: :info"
       end)
 
-      assert_file("phx_blog/config/runtime.exs", ~r/ip: {0, 0, 0, 0, 0, 0, 0, 0}/)
+      assert_file("phx_blog/config/runtime.exs", fn file ->
+        assert file =~
+                 ~r/^  http: \[port: String.to_integer\(System.get_env\("PORT", "4000"\)\)\]$/m
+
+        assert file =~ ~r/^\s+ip: {0, 0, 0, 0, 0, 0, 0, 0}$/m
+      end)
 
       assert_file("phx_blog/lib/phx_blog/application.ex", ~r/defmodule PhxBlog.Application do/)
       assert_file("phx_blog/lib/phx_blog.ex", ~r/defmodule PhxBlog do/)
@@ -147,7 +152,7 @@ defmodule Mix.Tasks.Phx.NewTest do
         assert file =~ "esbuild: {Esbuild,"
         assert file =~ "lib/phx_blog_web/router\\.ex$"
         assert file =~ "lib/phx_blog_web/(controllers|live|components)/.*\\.(ex|heex)$"
-        assert file =~ "http: [ip: {127, 0, 0, 1}"
+        assert file =~ "http: [ip: {127, 0, 0, 1}]"
       end)
 
       # tailwind
diff --git a/lib/mix/tasks/phx.gen.cert.ex b/lib/mix/tasks/phx.gen.cert.ex
index 46d1f44404..232bf1e486 100644
--- a/lib/mix/tasks/phx.gen.cert.ex
+++ b/lib/mix/tasks/phx.gen.cert.ex
@@ -122,7 +122,7 @@ defmodule Mix.Tasks.Phx.Gen.Cert do
     configuration in config/dev.exs:
 
       config #{inspect(app)}, #{inspect(Mix.Phoenix.web_module(base))}.Endpoint,
-        http: [port: String.to_integer(System.get_env("PORT") || "4000")],
+        ...,
         https: [
           port: 4001,
           cipher_suite: :strong,