diff --git a/packages/react-dom-bindings/src/server/ReactFizzConfigDOM.js b/packages/react-dom-bindings/src/server/ReactFizzConfigDOM.js
index 54504deb6e517..8a670f84592a9 100644
--- a/packages/react-dom-bindings/src/server/ReactFizzConfigDOM.js
+++ b/packages/react-dom-bindings/src/server/ReactFizzConfigDOM.js
@@ -431,9 +431,13 @@ export function createRenderState(
         fontPreloads: '',
         highImagePreloads: '',
         remainingCapacity:
-          typeof maxHeadersLength === 'number'
+          // We seed the remainingCapacity with 2 extra bytes because when we decrement the capacity
+          // we always assume we are inserting an interstitial ", " however the first header does not actually
+          // consume these two extra bytes.
+          2 +
+          (typeof maxHeadersLength === 'number'
             ? maxHeadersLength
-            : DEFAULT_HEADERS_CAPACITY_IN_UTF16_CODE_UNITS,
+            : DEFAULT_HEADERS_CAPACITY_IN_UTF16_CODE_UNITS),
       }
     : null;
   const renderState: RenderState = {
@@ -2953,7 +2957,7 @@ function pushImg(
         // make this behavior different between render and prerender since in the latter case
         // we are less sensitive to the current requests runtime per and more sensitive to maximizing
         // headers.
-        (headers.remainingCapacity -= header.length) >= 2)
+        (headers.remainingCapacity -= header.length + 2) >= 0)
       ) {
         // If we postpone in the shell we will still emit this preload so we track
         // it to make sure we don't reset it.
@@ -5393,7 +5397,7 @@ function prefetchDNS(href: string) {
         // make this behavior different between render and prerender since in the latter case
         // we are less sensitive to the current requests runtime per and more sensitive to maximizing
         // headers.
-        (headers.remainingCapacity -= header.length) >= 2)
+        (headers.remainingCapacity -= header.length + 2) >= 0)
       ) {
         // Store this as resettable in case we are prerendering and postpone in the Shell
         renderState.resets.dns[key] = EXISTS;
@@ -5452,7 +5456,7 @@ function preconnect(href: string, crossOrigin: ?CrossOriginEnum) {
         // make this behavior different between render and prerender since in the latter case
         // we are less sensitive to the current requests runtime per and more sensitive to maximizing
         // headers.
-        (headers.remainingCapacity -= header.length) >= 2)
+        (headers.remainingCapacity -= header.length + 2) >= 0)
       ) {
         // Store this in resettableState in case we are prerending and postpone in the Shell
         renderState.resets.connect[bucket][key] = EXISTS;
@@ -5518,7 +5522,7 @@ function preload(href: string, as: string, options?: ?PreloadImplOptions) {
           // make this behavior different between render and prerender since in the latter case
           // we are less sensitive to the current requests runtime per and more sensitive to maximizing
           // headers.
-          (headers.remainingCapacity -= header.length) >= 2)
+          (headers.remainingCapacity -= header.length + 2) >= 0)
         ) {
           // If we postpone in the shell we will still emit a preload as a header so we
           // track this to make sure we don't reset it.
@@ -5633,7 +5637,7 @@ function preload(href: string, as: string, options?: ?PreloadImplOptions) {
           // make this behavior different between render and prerender since in the latter case
           // we are less sensitive to the current requests runtime per and more sensitive to maximizing
           // headers.
-          (headers.remainingCapacity -= header.length) >= 2)
+          (headers.remainingCapacity -= header.length + 2) >= 0)
         ) {
           // If we postpone in the shell we will still emit this preload so we
           // track it here to prevent it from being reset.
@@ -6260,7 +6264,7 @@ export function emitEarlyPreloads(
             // This means that a particularly long header might close out the header queue where later
             // headers could still fit. We could in the future alter the behavior here based on prerender vs render
             // since during prerender we aren't as concerned with pure runtime performance.
-            if ((headers.remainingCapacity -= header.length) >= 2) {
+            if ((headers.remainingCapacity -= header.length + 2) >= 0) {
               renderState.resets.style[key] = PRELOAD_NO_CREDS;
               if (linkHeader) {
                 linkHeader += ', ';
diff --git a/packages/react-dom/src/__tests__/ReactDOMFizzServer-test.js b/packages/react-dom/src/__tests__/ReactDOMFizzServer-test.js
index f895bbd55e71b..f51101b4d40b6 100644
--- a/packages/react-dom/src/__tests__/ReactDOMFizzServer-test.js
+++ b/packages/react-dom/src/__tests__/ReactDOMFizzServer-test.js
@@ -3940,6 +3940,59 @@ describe('ReactDOMFizzServer', () => {
     expect(getVisibleChildren(container)).toEqual(<div>hello</div>);
   });
 
+  it('accounts for the length of the interstitial between links when computing the headers length', async () => {
+    let headers = null;
+    function onHeaders(x) {
+      headers = x;
+    }
+
+    function App() {
+      // 20 bytes
+      ReactDOM.preconnect('01');
+      // 42 bytes
+      ReactDOM.preconnect('02');
+      // 64 bytes
+      ReactDOM.preconnect('03');
+      // 86 bytes
+      ReactDOM.preconnect('04');
+      // 108 bytes
+      ReactDOM.preconnect('05');
+      // 130 bytes
+      ReactDOM.preconnect('06');
+      // 152 bytes
+      ReactDOM.preconnect('07');
+      // 174 bytes
+      ReactDOM.preconnect('08');
+      // 196 bytes
+      ReactDOM.preconnect('09');
+      // 218 bytes
+      ReactDOM.preconnect('10');
+      // 240 bytes
+      ReactDOM.preconnect('11');
+      // 262 bytes
+      ReactDOM.preconnect('12');
+      // 284 bytes
+      ReactDOM.preconnect('13');
+      // 306 bytes
+      ReactDOM.preconnect('14');
+      return (
+        <html>
+          <body>hello</body>
+        </html>
+      );
+    }
+
+    await act(() => {
+      renderToPipeableStream(<App />, {onHeaders, maxHeadersLength: 305});
+    });
+    expect(headers.Link.length).toBe(284);
+
+    await act(() => {
+      renderToPipeableStream(<App />, {onHeaders, maxHeadersLength: 306});
+    });
+    expect(headers.Link.length).toBe(306);
+  });
+
   describe('error escaping', () => {
     it('escapes error hash, message, and component stack values in directly flushed errors (html escaping)', async () => {
       window.__outlet = {};