diff --git a/lib/mcp/server.rb b/lib/mcp/server.rb
index 910c8d8f..d1800d1c 100644
--- a/lib/mcp/server.rb
+++ b/lib/mcp/server.rb
@@ -615,23 +615,32 @@ def handle_request(request, method, session: nil, related_request_id: nil)
     # Lifts the SEP-2575 per-request `_meta` envelope for modern requests. Only a request whose `_meta` carries
     # the full required triple is classified as modern; a partial triple keeps flowing through the legacy path untouched.
     # Notifications carry no envelope (their `_meta` is a `NotificationMetaObject`), and `server/discover` is
-    # pre-version discovery, so both are exempt. On a session already era-locked to modern, `initialize` is
-    # rejected with `-32022` (the modern lifecycle has no handshake) and the triple becomes required for
-    # every other request.
+    # pre-version discovery, so both are exempt. Era-locked sessions additionally enforce the dual-era rules:
+    # on a modern session, `initialize` is rejected with `-32022` (the modern lifecycle has no handshake)
+    # and the triple becomes required for every other request; on a legacy session, a modern envelope is rejected as
+    # an invalid request because a connection can never change eras.
     def lift_request_envelope(params, method:, session:)
       return if Methods.notification?(method)
       return if method == Methods::SERVER_DISCOVER
 
-      modern_session = session.respond_to?(:era) && session.era == :modern
+      era = session.respond_to?(:era) ? session.era : nil
 
-      if modern_session && method == Methods::INITIALIZE
+      if era == :modern && method == Methods::INITIALIZE
         requested = params.is_a?(Hash) ? params[:protocolVersion] || params["protocolVersion"] : nil
         raise UnsupportedProtocolVersionError.new(requested, params)
       end
 
       if RequestEnvelope.modern?(params)
+        if era == :legacy
+          raise RequestHandlerError.new(
+            "Invalid Request: the session already negotiated the legacy lifecycle via `initialize`",
+            params,
+            error_type: :invalid_request,
+          )
+        end
+
         RequestEnvelope.parse!(params, request: params)
-      elsif modern_session
+      elsif era == :modern
         raise RequestHandlerError.new(
           "Invalid Request: modern sessions require the SEP-2575 `_meta` envelope",
           params,
diff --git a/lib/mcp/server/transports/stdio_transport.rb b/lib/mcp/server/transports/stdio_transport.rb
index ec2bd6dd..8c758124 100644
--- a/lib/mcp/server/transports/stdio_transport.rb
+++ b/lib/mcp/server/transports/stdio_transport.rb
@@ -49,7 +49,9 @@ def open
             end
             break if line.nil?
 
-            response = @session.handle_json(line.strip)
+            line = line.strip
+            parsed = parse_line(line)
+            response = parsed ? dispatch_with_era(parsed) : @session.handle_json(line)
             send_response(response) if response
           end
         rescue Interrupt
@@ -90,6 +92,12 @@ def send_notification(method, params = nil)
         # cancellation has very limited value here regardless; servers that need cancellation propagation for nested
         # server-to-client requests should use `StreamableHTTPTransport`.
         def send_request(method, params = nil)
+          # The modern lifecycle (SEP-2575) forbids server-initiated JSON-RPC requests;
+          # multi round-trip `input_required` results (SEP-2322) replace them.
+          if @session && @session.era == :modern
+            raise "Server-initiated requests are not available in the modern lifecycle (SEP-2575)."
+          end
+
           request_id = generate_request_id
           request = { jsonrpc: "2.0", id: request_id, method: method }
           request[:params] = params if params
@@ -116,7 +124,7 @@ def send_request(method, params = nil)
 
               return parsed[:result]
             else
-              response = @session ? @session.handle(parsed) : @server.handle(parsed)
+              response = @session ? dispatch_with_era(parsed) : @server.handle(parsed)
               send_response(response) if response
             end
           end
@@ -143,6 +151,35 @@ def read_line(io)
 
           line
         end
+
+        # Parses a frame once so era classification can inspect its method and `_meta`.
+        # Returns `nil` for frames that are not JSON objects; those fall back to
+        # `ServerSession#handle_json` so protocol-level error responses stay identical.
+        def parse_line(line)
+          parsed = JSON.parse(line, symbolize_names: true)
+          parsed.is_a?(Hash) ? parsed : nil
+        rescue JSON::ParserError
+          nil
+        end
+
+        # Serves one frame under the dual-era model (SEP-2575): the first era-distinctive message to succeed locks
+        # the connection era. A successful `initialize` locks `:legacy` inside `Server#init`; a successful `server/discover`
+        # or a successful request carrying the full modern `_meta` triple locks `:modern`. Era-violating frames
+        # (an `initialize` after a modern lock, a modern envelope after a legacy lock, or a missing envelope after a modern lock)
+        # are rejected in-band by `Server#lift_request_envelope`.
+        def dispatch_with_era(parsed)
+          response = @session.handle(parsed)
+          lock_modern_era_on_success(parsed, response)
+          response
+        end
+
+        def lock_modern_era_on_success(parsed, response)
+          return if @session.era
+          return if !response.is_a?(Hash) || response.key?(:error)
+          return if parsed[:method] != Methods::SERVER_DISCOVER && !RequestEnvelope.modern?(parsed[:params])
+
+          @session.lock_era!(:modern)
+        end
       end
     end
   end
diff --git a/test/mcp/server/transports/stdio_transport_test.rb b/test/mcp/server/transports/stdio_transport_test.rb
index cdca209e..1b7d66d3 100644
--- a/test/mcp/server/transports/stdio_transport_test.rb
+++ b/test/mcp/server/transports/stdio_transport_test.rb
@@ -7,6 +7,7 @@ class Server
     module Transports
       class StdioTransportTest < ActiveSupport::TestCase
         include InstrumentationTestHelper
+        include InitializeParamsTestHelper
 
         setup do
           configuration = MCP::Configuration.new
@@ -550,6 +551,140 @@ class StdioTransportTest < ActiveSupport::TestCase
             $stdout = original_stdout
           end
         end
+
+        test "locks the legacy era on a successful initialize and rejects a later modern envelope" do
+          responses = run_transport_session([
+            initialize_request(id: 1),
+            modern_ping_request(id: 2),
+          ])
+
+          refute responses[0].key?(:error)
+          assert_equal :legacy, session_era
+          assert_equal JsonRpcHandler::ErrorCode::INVALID_REQUEST, responses[1].dig(:error, :code)
+        end
+
+        test "initialize negotiating 2026-07-28 still locks the legacy era" do
+          # 2026-07-28 serves both lifecycles of the dual-era model: negotiating it through
+          # the legacy handshake locks `:legacy`, so a later modern envelope is still rejected.
+          responses = run_transport_session([
+            initialize_request(id: 1, protocol_version: "2026-07-28"),
+            modern_ping_request(id: 2),
+          ])
+
+          assert_equal "2026-07-28", responses[0].dig(:result, :protocolVersion)
+          assert_equal :legacy, session_era
+          assert_equal JsonRpcHandler::ErrorCode::INVALID_REQUEST, responses[1].dig(:error, :code)
+        end
+
+        test "locks the modern era on a successful server/discover and rejects a later initialize with -32022" do
+          responses = run_transport_session([
+            { jsonrpc: "2.0", method: "server/discover", id: 1 },
+            initialize_request(id: 2),
+            modern_ping_request(id: 3),
+          ])
+
+          assert_equal Configuration::SUPPORTED_STABLE_PROTOCOL_VERSIONS, responses[0].dig(:result, :supportedVersions)
+          assert_equal :modern, session_era
+          assert_equal ErrorCodes::UNSUPPORTED_PROTOCOL_VERSION, responses[1].dig(:error, :code)
+          assert_equal Configuration::SUPPORTED_MODERN_PROTOCOL_VERSIONS, responses[1].dig(:error, :data, :supported)
+          refute responses[2].key?(:error)
+        end
+
+        test "locks the modern era on a successful request carrying the modern envelope" do
+          responses = run_transport_session([modern_ping_request(id: 1)])
+
+          refute responses[0].key?(:error)
+          assert_equal :modern, session_era
+        end
+
+        test "does not lock an era when the era-distinctive request fails" do
+          # An unsupported envelope version fails with -32022, so the connection stays unlocked
+          # and a legacy initialize can still succeed afterwards.
+          responses = run_transport_session([
+            modern_ping_request(id: 1, version: "2027-01-01"),
+            initialize_request(id: 2),
+          ])
+
+          assert_equal ErrorCodes::UNSUPPORTED_PROTOCOL_VERSION, responses[0].dig(:error, :code)
+          refute responses[1].key?(:error)
+          assert_equal :legacy, session_era
+        end
+
+        test "requires the modern envelope after a modern era lock" do
+          responses = run_transport_session([
+            modern_ping_request(id: 1),
+            { jsonrpc: "2.0", method: "ping", id: 2 },
+          ])
+
+          refute responses[0].key?(:error)
+          assert_equal JsonRpcHandler::ErrorCode::INVALID_REQUEST, responses[1].dig(:error, :code)
+        end
+
+        test "#send_request raises on a modern-locked session" do
+          run_transport_session([modern_ping_request(id: 1)])
+
+          error = assert_raises(RuntimeError) do
+            @transport.send_request("roots/list")
+          end
+          assert_match(/modern lifecycle/, error.message)
+        end
+
+        private
+
+        def initialize_request(id:, protocol_version: "2025-11-25")
+          {
+            jsonrpc: "2.0",
+            method: "initialize",
+            id: id,
+            params: initialize_params(
+              protocolVersion: protocol_version,
+              clientInfo: { name: "legacy_client", version: "1.0" },
+            ),
+          }
+        end
+
+        def modern_ping_request(id:, version: "2026-07-28")
+          {
+            jsonrpc: "2.0",
+            method: "ping",
+            id: id,
+            params: {
+              _meta: {
+                "io.modelcontextprotocol/protocolVersion": version,
+                "io.modelcontextprotocol/clientInfo": { name: "modern_client", version: "2.0" },
+                "io.modelcontextprotocol/clientCapabilities": {},
+              },
+            },
+          }
+        end
+
+        # Feeds the frames to a fresh transport session over swapped stdio and returns the parsed responses in order.
+        def run_transport_session(frames)
+          input = StringIO.new(frames.map { |frame| JSON.generate(frame) }.join("\n") + "\n")
+          output = StringIO.new
+
+          original_stdin = $stdin
+          original_stdout = $stdout
+
+          begin
+            $stdin = input
+            $stdout = output
+
+            thread = Thread.new { @transport.open }
+            sleep(0.1)
+            @transport.close
+            thread.join
+          ensure
+            $stdin = original_stdin
+            $stdout = original_stdout
+          end
+
+          output.string.each_line.map { |line| JSON.parse(line, symbolize_names: true) }
+        end
+
+        def session_era
+          @transport.instance_variable_get(:@session).era
+        end
       end
     end
   end