diff --git a/doc/api/cli.md b/doc/api/cli.md
index 47e86d0c324395..befab1aef586b5 100644
--- a/doc/api/cli.md
+++ b/doc/api/cli.md
@@ -2868,12 +2868,15 @@ The following values are valid for `mode`:
 ### `--use-system-ca`
 
 Node.js uses the trusted CA certificates present in the system store along with
-the `--use-bundled-ca`, `--use-openssl-ca` options.
+the `--use-bundled-ca` option and the `NODE_EXTRA_CA_CERTS` environment variable.
+On platforms other than Windows and macOS, this loads certificates from the directory
+and file trusted by OpenSSL, similar to `--use-openssl-ca`, with the difference being
+that it caches the certificates after first load.
 
-This option is only supported on Windows and macOS, and the certificate trust policy
-is planned to follow [Chromium's policy for locally trusted certificates][]:
+On Windows and macOS, the certificate trust policy is planned to follow
+[Chromium's policy for locally trusted certificates][]:
 
-On macOS, the following certifcates are trusted:
+On macOS, the following settings are respected:
 
 * Default and System Keychains
   * Trust:
@@ -2883,8 +2886,8 @@ On macOS, the following certifcates are trusted:
     * Any certificate where the “When using this certificate” flag is set to “Never Trust” or
     * Any certificate where the “Secure Sockets Layer (SSL)” flag is set to “Never Trust.”
 
-On Windows, the following certificates are currently trusted (unlike
-Chromium's policy, distrust is not currently supported):
+On Windows, the following settings are respected (unlike Chromium's policy, distrust
+and intermediate CA are not currently supported):
 
 * Local Machine (accessed via `certlm.msc`)
   * Trust:
@@ -2899,8 +2902,19 @@ Chromium's policy, distrust is not currently supported):
     * Trusted Root Certification Authorities
     * Enterprise Trust -> Group Policy -> Trusted Root Certification Authorities
 
-On any supported system, Node.js would check that the certificate's key usage and extended key
-usage are consistent with TLS use cases before using it for server authentication.
+On Windows and macOS, Node.js would check that the user settings for the certificates
+do not forbid them for TLS server authentication before using them.
+
+On other systems, Node.js loads certificates from the default certificate file
+(typically `/etc/ssl/cert.pem`) and default certificate directory (typically
+`/etc/ssl/certs`) that the version of OpenSSL that Node.js links to respects.
+This typically works with the convention on major Linux distributions and other
+Unix-like systems. If the overriding OpenSSL environment variables
+(typically `SSL_CERT_FILE` and `SSL_CERT_DIR`, depending on the configuration
+of the OpenSSL that Node.js links to) are set, the specified paths will be used to load
+certificates instead. These environment variables can be used as workarounds
+if the conventional paths used by the version of OpenSSL Node.js links to are
+not consistent with the system configuration that the users have for some reason.
 
 ### `--v8-options`
 
@@ -3541,7 +3555,8 @@ variable is ignored.
 added: v7.7.0
 -->
 
-If `--use-openssl-ca` is enabled, this overrides and sets OpenSSL's directory
+If `--use-openssl-ca` is enabled, or if `--use-system-ca` is enabled on
+platforms other than macOS and Windows, this overrides and sets OpenSSL's directory
 containing trusted certificates.
 
 Be aware that unless the child environment is explicitly set, this environment
@@ -3554,7 +3569,8 @@ may cause them to trust the same CAs as node.
 added: v7.7.0
 -->
 
-If `--use-openssl-ca` is enabled, this overrides and sets OpenSSL's file
+If `--use-openssl-ca` is enabled, or if `--use-system-ca` is enabled on
+platforms other than macOS and Windows, this overrides and sets OpenSSL's file
 containing trusted certificates.
 
 Be aware that unless the child environment is explicitly set, this environment
diff --git a/src/crypto/crypto_context.cc b/src/crypto/crypto_context.cc
index 28dedf33b18154..3e4b517fa462ef 100644
--- a/src/crypto/crypto_context.cc
+++ b/src/crypto/crypto_context.cc
@@ -223,7 +223,7 @@ int SSL_CTX_use_certificate_chain(SSL_CTX* ctx,
                                        issuer);
 }
 
-unsigned long LoadCertsFromFile(  // NOLINT(runtime/int)
+static unsigned long LoadCertsFromFile(  // NOLINT(runtime/int)
     std::vector<X509*>* certs,
     const char* file) {
   MarkPopErrorOnReturn mark_pop_error_on_return;
@@ -645,6 +645,74 @@ void ReadWindowsCertificates(
 }
 #endif
 
+static void LoadCertsFromDir(std::vector<X509*>* certs,
+                             std::string_view cert_dir) {
+  uv_fs_t dir_req;
+  auto cleanup = OnScopeLeave([&dir_req]() { uv_fs_req_cleanup(&dir_req); });
+  int err = uv_fs_scandir(nullptr, &dir_req, cert_dir.data(), 0, nullptr);
+  if (err < 0) {
+    fprintf(stderr,
+            "Cannot open directory %s to load OpenSSL certificates.\n",
+            cert_dir.data());
+    return;
+  }
+
+  uv_fs_t stats_req;
+  auto cleanup_stats =
+      OnScopeLeave([&stats_req]() { uv_fs_req_cleanup(&stats_req); });
+  for (;;) {
+    uv_dirent_t ent;
+
+    int r = uv_fs_scandir_next(&dir_req, &ent);
+    if (r == UV_EOF) {
+      break;
+    }
+    if (r < 0) {
+      char message[64];
+      uv_strerror_r(r, message, sizeof(message));
+      fprintf(stderr,
+              "Cannot scan directory %s to load OpenSSL certificates.\n",
+              cert_dir.data());
+      return;
+    }
+
+    std::string file_path = std::string(cert_dir) + "/" + ent.name;
+    int stats_r = uv_fs_stat(nullptr, &stats_req, file_path.c_str(), nullptr);
+    if (stats_r == 0 &&
+        (static_cast<uv_stat_t*>(stats_req.ptr)->st_mode & S_IFREG)) {
+      LoadCertsFromFile(certs, file_path.c_str());
+    }
+  }
+}
+
+// Loads CA certificates from the default certificate paths respected by
+// OpenSSL.
+void GetOpenSSLSystemCertificates(std::vector<X509*>* system_store_certs) {
+  std::string cert_file;
+  // While configurable when OpenSSL is built, this is usually SSL_CERT_FILE.
+  if (!credentials::SafeGetenv(X509_get_default_cert_file_env(), &cert_file)) {
+    // This is usually /etc/ssl/cert.pem if we are using the OpenSSL statically
+    // linked and built with default configurations.
+    cert_file = X509_get_default_cert_file();
+  }
+
+  std::string cert_dir;
+  // While configurable when OpenSSL is built, this is usually SSL_CERT_DIR.
+  if (!credentials::SafeGetenv(X509_get_default_cert_dir_env(), &cert_dir)) {
+    // This is usually /etc/ssl/certs if we are using the OpenSSL statically
+    // linked and built with default configurations.
+    cert_dir = X509_get_default_cert_dir();
+  }
+
+  if (!cert_file.empty()) {
+    LoadCertsFromFile(system_store_certs, cert_file.c_str());
+  }
+
+  if (!cert_dir.empty()) {
+    LoadCertsFromDir(system_store_certs, cert_dir.c_str());
+  }
+}
+
 static std::vector<X509*> InitializeBundledRootCertificates() {
   // Read the bundled certificates in node_root_certs.h into
   // bundled_root_certs_vector.
@@ -685,6 +753,9 @@ static std::vector<X509*> InitializeSystemStoreCertificates() {
 #endif
 #ifdef _WIN32
   ReadWindowsCertificates(&system_store_certs);
+#endif
+#if !defined(__APPLE__) && !defined(_WIN32)
+  GetOpenSSLSystemCertificates(&system_store_certs);
 #endif
   return system_store_certs;
 }
diff --git a/test/parallel/test-native-certs.mjs b/test/parallel/test-native-certs.mjs
index f27e1d81a4f05e..ed8769e92acb32 100644
--- a/test/parallel/test-native-certs.mjs
+++ b/test/parallel/test-native-certs.mjs
@@ -7,10 +7,6 @@ import fixtures from '../common/fixtures.js';
 import { it, beforeEach, afterEach, describe } from 'node:test';
 import { once } from 'events';
 
-if (!common.isMacOS && !common.isWindows) {
-  common.skip('--use-system-ca is only supported on macOS and Windows');
-}
-
 if (!common.hasCrypto) {
   common.skip('requires crypto');
 }
@@ -34,6 +30,19 @@ if (!common.hasCrypto) {
 //    $  $thumbprint = (Get-ChildItem -Path Cert:\CurrentUser\Root | \
 //          Where-Object { $_.Subject -match "StartCom Certification Authority" }).Thumbprint
 //    $  Remove-Item -Path "Cert:\CurrentUser\Root\$thumbprint"
+//
+// On Debian/Ubuntu:
+//   1. To add the certificate:
+//     $ sudo cp test/fixtures/keys/fake-startcom-root-cert.pem \
+//       /usr/local/share/ca-certificates/fake-startcom-root-cert.crt
+//     $ sudo update-ca-certificates
+//   2. To remove the certificate
+//     $ sudo rm /usr/local/share/ca-certificates/fake-startcom-root-cert.crt
+//     $ sudo update-ca-certificates --fresh
+//
+// For other Unix-like systems, consult their manuals, there are usually
+// file-based processes similar to the Debian/Ubuntu one but with different
+// file locations and update commands.
 const handleRequest = (req, res) => {
   const path = req.url;
   switch (path) {