diff --git a/doc/api/http2.md b/doc/api/http2.md
index f5dbe67fc514..b7fee4396ca5 100644
--- a/doc/api/http2.md
+++ b/doc/api/http2.md
@@ -669,10 +669,16 @@ added:
 
 * `windowSize` {number}
 
-Sets the local endpoint's window size.
+Sets the local endpoint's connection-level window size.
 The `windowSize` is the total window size to set, not
 the delta.
 
+Increases take effect immediately, but decreases only apply as the window
+already advertised to the peer is consumed, since a window that has been
+advertised cannot be retracted. To use a window smaller than the default from
+the start of the connection, set the `connectionWindowSize` option when
+creating the server or client session instead.
+
 ```mjs
 import { createServer } from 'node:http2';
 
@@ -2844,6 +2850,9 @@ Throws `ERR_INVALID_ARG_TYPE` for invalid `settings` argument.
 <!-- YAML
 added: v8.4.0
 changes:
+  - version: REPLACEME
+    pr-url: https://github.com/nodejs/node/pull/65619
+    description: Added the `connectionWindowSize` option.
   - version:
      - v25.7.0
      - v24.15.0
@@ -2961,6 +2970,13 @@ changes:
     error that should tell the peer to not open any more streams, continuing
     to open streams is therefore regarded as a sign of a misbehaving peer.
     **Default:** `100`.
+  * `connectionWindowSize` {number} Sets the initial flow control window for
+    each session, in bytes. This is the total amount of data the remote peer
+    may send across all streams before it has to wait for a `WINDOW_UPDATE`.
+    The equivalent per-stream limit is `settings.initialWindowSize`. The
+    minimum allowed value is `1` and the maximum is 2<sup>31</sup>-1. Values
+    below 65535 will not take effect until the initial protocol-default
+    window of 65535 has been used.
   * `settings` {HTTP/2 Settings Object} The initial settings to send to the
     remote peer upon connection.
   * `streamResetBurst` {number} and `streamResetRate` {number} Sets the rate
@@ -3072,6 +3088,9 @@ server.listen(8000);
 <!-- YAML
 added: v8.4.0
 changes:
+  - version: REPLACEME
+    pr-url: https://github.com/nodejs/node/pull/65619
+    description: Added the `connectionWindowSize` option.
   - version:
      - v25.7.0
      - v24.15.0
@@ -3180,6 +3199,14 @@ changes:
     error that should tell the peer to not open any more streams, continuing
     to open streams is therefore regarded as a sign of a misbehaving peer.
     **Default:** `100`.
+  * `connectionWindowSize` {number} Sets the initial flow control window for
+    each session, in bytes. This is the total amount of data the remote peer
+    may send across all streams before it has to wait for a `WINDOW_UPDATE`.
+    The equivalent per-stream limit is `settings.initialWindowSize`. The
+    minimum allowed value is `1` and the maximum is 2<sup>31</sup>-1. Values
+    below 65535 will not take effect until the initial protocol-default
+    window of 65535 has been used.
+    **Default:** `33554432`.
   * `settings` {HTTP/2 Settings Object} The initial settings to send to the
     remote peer upon connection.
   * `streamResetBurst` {number} and `streamResetRate` {number} Sets the rate
@@ -3276,6 +3303,9 @@ server.listen(8443);
 <!-- YAML
 added: v8.4.0
 changes:
+  - version: REPLACEME
+    pr-url: https://github.com/nodejs/node/pull/65619
+    description: Added the `connectionWindowSize` option.
   - version:
       - v15.10.0
       - v14.16.0
@@ -3363,6 +3393,14 @@ changes:
   * `protocol` {string} The protocol to connect with, if not set in the
     `authority`. Value may be either `'http:'` or `'https:'`. **Default:**
     `'https:'`
+  * `connectionWindowSize` {number} Sets the initial flow control window for
+    this session, in bytes. This is the total amount of data the remote peer
+    may send across all streams before it has to wait for a `WINDOW_UPDATE`.
+    The equivalent per-stream limit is `settings.initialWindowSize`. The
+    minimum allowed value is `1` and the maximum is 2<sup>31</sup>-1. Values
+    below 65535 will not take effect until the initial protocol-default
+    window of 65535 has been used.
+    **Default:** `33554432`.
   * `settings` {HTTP/2 Settings Object} The initial settings to send to the
     remote peer upon connection.
   * `remoteCustomSettings` {Array} The array of integer values determines the
@@ -3795,6 +3833,9 @@ properties.
 * `initialWindowSize` {number} Specifies the _sender's_ initial window size in
   bytes for stream-level flow control. The minimum allowed value is 0. The
   maximum allowed value is 2<sup>32</sup>-1. **Default:** `4194304`.
+  This is a per-stream limit; the window for the connection as a whole is
+  configured separately with the `connectionWindowSize` option of
+  [`http2.createServer()`][] or [`http2.connect()`][].
 * `maxFrameSize` {number} Specifies the size in bytes of the largest frame
   payload. The minimum allowed value is 16,384. The maximum allowed value is
   2<sup>24</sup>-1. **Default:** `16384`.
@@ -5252,6 +5293,7 @@ you need to implement any fall-back behavior yourself.
 [`http.createServer()`]: http.md#httpcreateserveroptions-requestlistener
 [`http2.SecureServer`]: #class-http2secureserver
 [`http2.Server`]: #class-http2server
+[`http2.connect()`]: #http2connectauthority-options-listener
 [`http2.createSecureServer()`]: #http2createsecureserveroptions-onrequesthandler
 [`http2.createServer()`]: #http2createserveroptions-onrequesthandler
 [`http2stream.pushStream()`]: #http2streampushstreamheaders-options-callback
diff --git a/lib/internal/http2/core.js b/lib/internal/http2/core.js
index 4700120b0dd4..ceb173aa04e6 100644
--- a/lib/internal/http2/core.js
+++ b/lib/internal/http2/core.js
@@ -241,6 +241,8 @@ function debugSessionObj(session, message, ...args) {
 const kMaxFrameSize = (2 ** 24) - 1;
 const kMaxInt = (2 ** 32) - 1;
 const kMaxInitialWindowSize = (2 ** 31) - 1;  // HTTP/2 spec maximum
+// A connection window of 0 stalls the connection
+const kMinConnectionWindowSize = 1;
 const kMaxStreams = (2 ** 32) - 1;
 const kMaxALTSVC = (2 ** 14) - 2;
 
@@ -3590,12 +3592,8 @@ function connectionListener(socket) {
   this.emit('session', session);
 }
 
-function initializeOptions(options) {
-  assertIsObject(options, 'options');
-  options = { ...options };
-  assertIsObject(options.settings, 'options.settings');
-  options.settings = { ...options.settings };
-
+// Validates the session options that apply to both client and server sessions
+function validateSessionOptions(options) {
   assertIsArray(options.remoteCustomSettings, 'options.remoteCustomSettings');
   if (options.remoteCustomSettings) {
     options.remoteCustomSettings = [ ...options.remoteCustomSettings ];
@@ -3603,6 +3601,29 @@ function initializeOptions(options) {
       throw new ERR_HTTP2_TOO_MANY_CUSTOM_SETTINGS();
   }
 
+  if (options.strictSingleValueFields !== undefined) {
+    validateBoolean(
+      options.strictSingleValueFields,
+      'options.strictSingleValueFields',
+    );
+  } else {
+    options.strictSingleValueFields = true;
+  }
+
+  if (options.connectionWindowSize !== undefined) {
+    validateInt32(options.connectionWindowSize, 'options.connectionWindowSize',
+                  kMinConnectionWindowSize, kMaxInitialWindowSize);
+  }
+}
+
+function initializeOptions(options) {
+  assertIsObject(options, 'options');
+  options = { ...options };
+  assertIsObject(options.settings, 'options.settings');
+  options.settings = { ...options.settings };
+
+  validateSessionOptions(options);
+
   if (options.maxSessionInvalidFrames !== undefined)
     validateUint32(options.maxSessionInvalidFrames, 'options.maxSessionInvalidFrames');
 
@@ -3619,16 +3640,6 @@ function initializeOptions(options) {
     // TODO(danbev): is this a good default value?
     options.unknownProtocolTimeout = 10000;
 
-  if (options.strictSingleValueFields !== undefined) {
-    validateBoolean(
-      options.strictSingleValueFields,
-      'options.strictSingleValueFields',
-    );
-  } else {
-    options.strictSingleValueFields = true;
-  }
-
-
   // Initialize http1Options bag for HTTP/1 fallback when allowHTTP1 is true.
   // This bag is passed to storeHTTPOptions() to configure HTTP/1 server
   // behavior (timeouts, IncomingMessage/ServerResponse classes, etc.).
@@ -3840,21 +3851,7 @@ function connect(authority, options, listener) {
     maxOriginSetSize = 128;
   }
 
-  assertIsArray(options.remoteCustomSettings, 'options.remoteCustomSettings');
-  if (options.remoteCustomSettings) {
-    options.remoteCustomSettings = [ ...options.remoteCustomSettings ];
-    if (options.remoteCustomSettings.length > MAX_ADDITIONAL_SETTINGS)
-      throw new ERR_HTTP2_TOO_MANY_CUSTOM_SETTINGS();
-  }
-
-  if (options.strictSingleValueFields !== undefined) {
-    validateBoolean(
-      options.strictSingleValueFields,
-      'options.strictSingleValueFields',
-    );
-  } else {
-    options.strictSingleValueFields = true;
-  }
+  validateSessionOptions(options);
 
   if (typeof authority === 'string')
     authority = new URL(authority);
diff --git a/lib/internal/http2/util.js b/lib/internal/http2/util.js
index 159ba5bd5315..e2e6288b9ec6 100644
--- a/lib/internal/http2/util.js
+++ b/lib/internal/http2/util.js
@@ -233,7 +233,8 @@ const IDX_OPTIONS_MAX_SETTINGS = 9;
 const IDX_OPTIONS_STREAM_RESET_RATE = 10;
 const IDX_OPTIONS_STREAM_RESET_BURST = 11;
 const IDX_OPTIONS_STRICT_HTTP_FIELD_WHITESPACE_VALIDATION = 12;
-const IDX_OPTIONS_FLAGS = 13;
+const IDX_OPTIONS_CONNECTION_WINDOW_SIZE = 13;
+const IDX_OPTIONS_FLAGS = 14;
 
 function updateOptionsBuffer(options) {
   let flags = 0;
@@ -303,6 +304,11 @@ function updateOptionsBuffer(options) {
     optionsBuffer[IDX_OPTIONS_STRICT_HTTP_FIELD_WHITESPACE_VALIDATION] =
       options.strictFieldWhitespaceValidation === true ? 0 : 1;
   }
+  if (typeof options.connectionWindowSize === 'number') {
+    flags |= (1 << IDX_OPTIONS_CONNECTION_WINDOW_SIZE);
+    optionsBuffer[IDX_OPTIONS_CONNECTION_WINDOW_SIZE] =
+      options.connectionWindowSize;
+  }
 
   optionsBuffer[IDX_OPTIONS_FLAGS] = flags;
 }
diff --git a/src/node_http2.cc b/src/node_http2.cc
index 4ce35dc37c23..f5018d10d7ee 100644
--- a/src/node_http2.cc
+++ b/src/node_http2.cc
@@ -217,6 +217,11 @@ Http2Options::Http2Options(Http2State* http2_state, SessionType type) {
         static_cast<size_t>(buffer[IDX_OPTIONS_MAX_SETTINGS]));
   }
 
+  if (flags & (1 << IDX_OPTIONS_CONNECTION_WINDOW_SIZE)) {
+    set_connection_window_size(
+        static_cast<int32_t>(buffer[IDX_OPTIONS_CONNECTION_WINDOW_SIZE]));
+  }
+
   if ((flags & (1 << IDX_OPTIONS_STREAM_RESET_BURST)) &&
       (flags & (1 << IDX_OPTIONS_STREAM_RESET_RATE))) {
     nghttp2_option_set_stream_reset_rate_limit(
@@ -612,15 +617,13 @@ Http2Session::Http2Session(Http2State* http2_state,
       &alloc_info), 0);
   session_.reset(session);
 
-  // Increase the default local connection window to improve throughput
-  // on high-latency connections. The default 64KB window limits throughput
-  // to window_size / RTT. With a 32MB connection window, throughput is
-  // significantly improved. See https://github.com/nodejs/node/issues/38426
+  // The default connection window is larger than the 64KB required by the
+  // spec to improve throughput on high-latency connections, where throughput
+  // is limited to window_size / RTT. User settings have to be applied here
+  // initially rather than updating later as windows cannot be shrunk after
+  // they've been advertised.
   CHECK_EQ(nghttp2_session_set_local_window_size(
-               session,
-               NGHTTP2_FLAG_NONE,
-               0,
-               DEFAULT_SETTINGS_LOCAL_CONNECTION_WINDOW_SIZE),
+               session, NGHTTP2_FLAG_NONE, 0, opts.connection_window_size()),
            0);
 
   outgoing_storage_.reserve(1024);
diff --git a/src/node_http2.h b/src/node_http2.h
index f3edcf658f80..c042c46ab595 100644
--- a/src/node_http2.h
+++ b/src/node_http2.h
@@ -39,6 +39,10 @@ constexpr size_t kDefaultMaxSettings = 10;
 // Default maximum total memory cap for Http2Session.
 constexpr uint64_t kDefaultMaxSessionMemory = 10000000;
 
+// Default connection-level flow control window (32MB) to improve throughput
+// on high-latency connections. See https://github.com/nodejs/node/issues/38426
+constexpr int32_t kDefaultConnectionWindowSize = 33554432;
+
 // These are the standard HTTP/2 defaults as specified by the RFC
 constexpr uint32_t DEFAULT_SETTINGS_HEADER_TABLE_SIZE = 4096;
 constexpr uint32_t DEFAULT_SETTINGS_ENABLE_PUSH = 1;
@@ -51,10 +55,6 @@ constexpr uint32_t MAX_MAX_FRAME_SIZE = 16777215;
 constexpr uint32_t MIN_MAX_FRAME_SIZE = DEFAULT_SETTINGS_MAX_FRAME_SIZE;
 constexpr uint32_t MAX_INITIAL_WINDOW_SIZE = 2147483647;
 
-// Default local connection window size (32MB) to improve throughput
-// on high-latency connections. See https://github.com/nodejs/node/issues/38426
-constexpr uint32_t DEFAULT_SETTINGS_LOCAL_CONNECTION_WINDOW_SIZE = 33554432;
-
 // Stream is not going to have any DATA frames
 constexpr int STREAM_OPTION_EMPTY_PAYLOAD = 0x1;
 
@@ -245,9 +245,16 @@ class Http2Options {
     return max_session_memory_;
   }
 
+  void set_connection_window_size(int32_t size) {
+    connection_window_size_ = size;
+  }
+
+  int32_t connection_window_size() const { return connection_window_size_; }
+
  private:
   Nghttp2OptionPointer options_;
   uint64_t max_session_memory_ = kDefaultMaxSessionMemory;
+  int32_t connection_window_size_ = kDefaultConnectionWindowSize;
   uint32_t max_header_pairs_ = DEFAULT_MAX_HEADER_LIST_PAIRS;
   PaddingStrategy padding_strategy_ = PADDING_STRATEGY_NONE;
   size_t max_outstanding_pings_ = kDefaultMaxPings;
diff --git a/src/node_http2_state.h b/src/node_http2_state.h
index 914ad011e021..33fe342fd0b7 100644
--- a/src/node_http2_state.h
+++ b/src/node_http2_state.h
@@ -61,6 +61,7 @@ namespace http2 {
     IDX_OPTIONS_STREAM_RESET_RATE,
     IDX_OPTIONS_STREAM_RESET_BURST,
     IDX_OPTIONS_STRICT_HTTP_FIELD_WHITESPACE_VALIDATION,
+    IDX_OPTIONS_CONNECTION_WINDOW_SIZE,
     IDX_OPTIONS_FLAGS
   };
 
diff --git a/test/parallel/test-http2-connection-window-size-option.js b/test/parallel/test-http2-connection-window-size-option.js
new file mode 100644
index 000000000000..ddf5932fb28d
--- /dev/null
+++ b/test/parallel/test-http2-connection-window-size-option.js
@@ -0,0 +1,108 @@
+'use strict';
+
+const common = require('../common');
+if (!common.hasCrypto)
+  common.skip('missing crypto');
+
+const assert = require('assert');
+const http2 = require('http2');
+
+const DEFAULT_WINDOW = 33554432;
+const SPEC_DEFAULT_WINDOW = 65535;
+
+// Set client & server's windows (or default if undefined) and validate that
+// the both peers see the remote value as expected.
+function check(serverWindow, clientWindow) {
+  const server = http2.createServer({ connectionWindowSize: serverWindow });
+  serverWindow ??= DEFAULT_WINDOW;
+  clientWindow ??= DEFAULT_WINDOW;
+
+  server.on('session', common.mustCall((session) => {
+    assert.strictEqual(session.state.effectiveLocalWindowSize, serverWindow);
+  }));
+
+  server.on('stream', common.mustCall((stream) => {
+    assert.strictEqual(stream.session.state.remoteWindowSize, clientWindow);
+    stream.respond({ ':status': 200 }, { endStream: true });
+  }));
+
+  server.listen(0, common.mustCall(() => {
+    const client = http2.connect(`http://localhost:${server.address().port}`,
+                                 { connectionWindowSize: clientWindow });
+
+    client.on('connect', common.mustCall(() => {
+      assert.strictEqual(client.state.effectiveLocalWindowSize, clientWindow);
+    }));
+
+    const req = client.request();
+    req.resume();
+    req.on('close', common.mustCall(() => {
+      assert.strictEqual(client.state.remoteWindowSize, serverWindow);
+      client.close();
+      server.close();
+    }));
+  }));
+}
+
+check(undefined, undefined);
+
+// The option shrinks the window below the default, which setLocalWindowSize()
+// cannot do once the connection has been established.
+check(SPEC_DEFAULT_WINDOW, SPEC_DEFAULT_WINDOW);
+
+// Each end of the connection is configured independently.
+check(2 ** 20, 2 ** 21);
+
+// A window below the peer's fixed initial 65535 is the only case that shrinks
+// the window nghttp2 has already accounted for, leaving a reduction to pay off
+// before any WINDOW_UPDATE can be sent again. Larger windows, including the
+// default, only ever grow it. Send more than the window to prove the
+// connection still resumes rather than stalling once the reduction is paid.
+{
+  const windowSize = 16384;
+  const payload = Buffer.alloc(2 ** 18, 'x');
+  const server = http2.createServer({ connectionWindowSize: windowSize });
+
+  server.on('stream', common.mustCall((stream) => {
+    let received = 0;
+    stream.on('data', (chunk) => { received += chunk.length; });
+    stream.on('end', common.mustCall(() => {
+      assert.strictEqual(received, payload.length);
+      stream.respond({ ':status': 200 }, { endStream: true });
+    }));
+  }));
+
+  server.listen(0, common.mustCall(() => {
+    const client = http2.connect(`http://localhost:${server.address().port}`,
+                                 { connectionWindowSize: windowSize });
+    const req = client.request({ ':method': 'POST', ':path': '/' });
+    req.resume();
+    req.end(payload);
+    req.on('close', common.mustCall(() => {
+      client.close();
+      server.close();
+    }));
+  }));
+}
+
+for (const connectionWindowSize of [-1, 0, 2 ** 31, 1.5]) {
+  assert.throws(() => http2.createServer({ connectionWindowSize }),
+                { code: 'ERR_OUT_OF_RANGE' });
+  assert.throws(() => http2.createSecureServer({ connectionWindowSize }),
+                { code: 'ERR_OUT_OF_RANGE' });
+  assert.throws(() => http2.connect('http://localhost:80', { connectionWindowSize }),
+                { code: 'ERR_OUT_OF_RANGE' });
+}
+
+// Windows below the peer's fixed initial 65535 are permitted: they cannot
+// shrink that first burst, but they do throttle everything after it.
+for (const connectionWindowSize of [1, 1024, 65534]) {
+  http2.createServer({ connectionWindowSize }).close();
+}
+
+for (const connectionWindowSize of ['1024', null, {}]) {
+  assert.throws(() => http2.createServer({ connectionWindowSize }),
+                { code: 'ERR_INVALID_ARG_TYPE' });
+  assert.throws(() => http2.connect('http://localhost:80', { connectionWindowSize }),
+                { code: 'ERR_INVALID_ARG_TYPE' });
+}
diff --git a/test/parallel/test-http2-util-update-options-buffer.js b/test/parallel/test-http2-util-update-options-buffer.js
index 888ddd287cf1..c046395f1a88 100644
--- a/test/parallel/test-http2-util-update-options-buffer.js
+++ b/test/parallel/test-http2-util-update-options-buffer.js
@@ -26,7 +26,8 @@ const IDX_OPTIONS_MAX_SETTINGS = 9;
 const IDX_OPTIONS_STREAM_RESET_RATE = 10;
 const IDX_OPTIONS_STREAM_RESET_BURST = 11;
 const IDX_OPTIONS_STRICT_HTTP_FIELD_WHITESPACE_VALIDATION = 12;
-const IDX_OPTIONS_FLAGS = 13;
+const IDX_OPTIONS_CONNECTION_WINDOW_SIZE = 13;
+const IDX_OPTIONS_FLAGS = 14;
 
 {
   updateOptionsBuffer({
@@ -42,7 +43,8 @@ const IDX_OPTIONS_FLAGS = 13;
     maxSettings: 10,
     streamResetRate: 11,
     streamResetBurst: 12,
-    strictFieldWhitespaceValidation: false
+    strictFieldWhitespaceValidation: false,
+    connectionWindowSize: 13
   });
 
   assert.strictEqual(optionsBuffer[IDX_OPTIONS_MAX_DEFLATE_DYNAMIC_TABLE_SIZE], 1);
@@ -58,6 +60,7 @@ const IDX_OPTIONS_FLAGS = 13;
   assert.strictEqual(optionsBuffer[IDX_OPTIONS_STREAM_RESET_RATE], 11);
   assert.strictEqual(optionsBuffer[IDX_OPTIONS_STREAM_RESET_BURST], 12);
   assert.strictEqual(optionsBuffer[IDX_OPTIONS_STRICT_HTTP_FIELD_WHITESPACE_VALIDATION], 1);
+  assert.strictEqual(optionsBuffer[IDX_OPTIONS_CONNECTION_WINDOW_SIZE], 13);
 
   const flags = optionsBuffer[IDX_OPTIONS_FLAGS];
 
@@ -73,11 +76,13 @@ const IDX_OPTIONS_FLAGS = 13;
   assert.ok(flags & (1 << IDX_OPTIONS_STREAM_RESET_RATE));
   assert.ok(flags & (1 << IDX_OPTIONS_STREAM_RESET_BURST));
   assert.ok(flags & (1 << IDX_OPTIONS_STRICT_HTTP_FIELD_WHITESPACE_VALIDATION));
+  assert.ok(flags & (1 << IDX_OPTIONS_CONNECTION_WINDOW_SIZE));
 }
 
 {
   optionsBuffer[IDX_OPTIONS_MAX_SEND_HEADER_BLOCK_LENGTH] = 0;
   optionsBuffer[IDX_OPTIONS_MAX_OUTSTANDING_PINGS] = 0;
+  optionsBuffer[IDX_OPTIONS_CONNECTION_WINDOW_SIZE] = 0;
 
   updateOptionsBuffer({
     maxDeflateDynamicTableSize: 1,
@@ -94,6 +99,7 @@ const IDX_OPTIONS_FLAGS = 13;
   assert.strictEqual(optionsBuffer[IDX_OPTIONS_MAX_HEADER_LIST_PAIRS], 6);
   assert.strictEqual(optionsBuffer[IDX_OPTIONS_MAX_SEND_HEADER_BLOCK_LENGTH], 0);
   assert.strictEqual(optionsBuffer[IDX_OPTIONS_MAX_OUTSTANDING_PINGS], 0);
+  assert.strictEqual(optionsBuffer[IDX_OPTIONS_CONNECTION_WINDOW_SIZE], 0);
 
   const flags = optionsBuffer[IDX_OPTIONS_FLAGS];
 
@@ -105,4 +111,5 @@ const IDX_OPTIONS_FLAGS = 13;
 
   assert.ok(!(flags & (1 << IDX_OPTIONS_MAX_SEND_HEADER_BLOCK_LENGTH)));
   assert.ok(!(flags & (1 << IDX_OPTIONS_MAX_OUTSTANDING_PINGS)));
+  assert.ok(!(flags & (1 << IDX_OPTIONS_CONNECTION_WINDOW_SIZE)));
 }