diff --git a/packages/miniflare/src/plugins/core/index.ts b/packages/miniflare/src/plugins/core/index.ts
index 97a9b73c4..b68b92aac 100644
--- a/packages/miniflare/src/plugins/core/index.ts
+++ b/packages/miniflare/src/plugins/core/index.ts
@@ -65,7 +65,12 @@ if (process.env.NODE_EXTRA_CA_CERTS !== undefined) {
   // https://nodejs.org/api/cli.html#node_extra_ca_certsfile
   try {
     const extra = readFileSync(process.env.NODE_EXTRA_CA_CERTS, "utf8");
-    trustedCertificates.push(extra);
+    // Split bundle into individual certificates and add each individually:
+    // https://github.com/cloudflare/miniflare/pull/587/files#r1271579671
+    const pemBegin = "-----BEGIN";
+    for (const cert of extra.split(pemBegin)) {
+      if (cert.trim() !== "") trustedCertificates.push(pemBegin + cert);
+    }
   } catch {}
 }
 
diff --git a/packages/miniflare/test/plugins/core/index.spec.ts b/packages/miniflare/test/plugins/core/index.spec.ts
new file mode 100644
index 000000000..07184d495
--- /dev/null
+++ b/packages/miniflare/test/plugins/core/index.spec.ts
@@ -0,0 +1,90 @@
+import childProcess from "child_process";
+import { once } from "events";
+import fs from "fs/promises";
+import https from "https";
+import { AddressInfo } from "net";
+import path from "path";
+import { text } from "stream/consumers";
+import tls from "tls";
+import test from "ava";
+import stoppable from "stoppable";
+import which from "which";
+import { useTmp } from "../../test-shared";
+
+const opensslInstalled = which.sync("openssl", { nothrow: true });
+const opensslTest = opensslInstalled ? test : test.skip;
+opensslTest("NODE_EXTRA_CA_CERTS: loads certificates", async (t) => {
+  const tmp = await useTmp(t);
+
+  // Generate self-signed certificate
+  childProcess.execSync(
+    'openssl req -newkey rsa:2048 -nodes -keyout key.pem -x509 -days 30 -out cert.pem -subj "/CN=localhost"',
+    { cwd: tmp, stdio: "ignore" }
+  );
+  const keyPath = path.join(tmp, "key.pem");
+  const certPath = path.join(tmp, "cert.pem");
+  const key = await fs.readFile(keyPath);
+  const cert = await fs.readFile(certPath);
+
+  // Start HTTPS server with self-signed certificate
+  const responseBody = "secure body";
+  const server = https.createServer({ key, cert }, (req, res) => {
+    res.end(responseBody);
+  });
+  const stoppableServer = stoppable(server, /* grace */ 0);
+  const url = await new Promise<string>((resolve) => {
+    server.listen(0, () => {
+      t.teardown(() => {
+        return new Promise((resolve, reject) =>
+          stoppableServer.stop((err) => (err ? reject(err) : resolve()))
+        );
+      });
+      const port = (server.address() as AddressInfo).port;
+      resolve(`https://localhost:${port}`);
+    });
+  });
+
+  // Write NODE_EXTRA_CA_CERTS file, with multiple certificates
+  // (see https://github.com/cloudflare/miniflare/pull/587/files#r1271579671)
+  const caCertsPath = path.join(tmp, "bundle.pem");
+  const caCerts = [...tls.rootCertificates, cert];
+  await fs.writeFile(caCertsPath, caCerts.join("\n"));
+
+  // Start Miniflare with NODE_EXTRA_CA_CERTS environment variable
+  // (cannot use sync process methods here as that would block HTTPS server)
+  const result = childProcess.spawn(
+    process.execPath,
+    [
+      "-e",
+      `
+      const { Miniflare } = require("miniflare");
+      const mf = new Miniflare({
+        verbose: true,
+        modules: true,
+        script: \`export default {
+          fetch() {
+            return fetch(${JSON.stringify(url)});
+          }
+        }\`
+      });
+      (async () => {
+        const res = await mf.dispatchFetch("http://placeholder/");
+        const text = await res.text();
+        console.log(text);
+        await mf.dispose();
+      })();
+      `,
+    ],
+    {
+      stdio: [/* in */ "ignore", /* out */ "pipe", /* error */ "inherit"],
+      env: { NODE_EXTRA_CA_CERTS: caCertsPath },
+    }
+  );
+
+  // Check response matches expected
+  const exitPromise = once(result, "exit");
+  const resultText = await text(result.stdout);
+  await exitPromise;
+  t.is(result.exitCode, 0);
+  t.is(resultText.trim(), responseBody);
+});