diff --git a/testing/web3signer_tests/src/lib.rs b/testing/web3signer_tests/src/lib.rs
index a58dcb5fa0..bebc8fa13b 100644
--- a/testing/web3signer_tests/src/lib.rs
+++ b/testing/web3signer_tests/src/lib.rs
@@ -130,7 +130,11 @@ mod tests {
     }
 
     fn client_identity_path() -> PathBuf {
-        tls_dir().join("lighthouse").join("key.p12")
+        if cfg!(target_os = "macos") {
+            tls_dir().join("lighthouse").join("key_legacy.p12")
+        } else {
+            tls_dir().join("lighthouse").join("key.p12")
+        }
     }
 
     fn client_identity_password() -> String {
diff --git a/testing/web3signer_tests/tls/generate.sh b/testing/web3signer_tests/tls/generate.sh
index f918e87cf8..3b14dbddba 100755
--- a/testing/web3signer_tests/tls/generate.sh
+++ b/testing/web3signer_tests/tls/generate.sh
@@ -1,7 +1,20 @@
 #!/bin/bash
-openssl req -x509 -sha256 -nodes -days 36500 -newkey rsa:4096 -keyout web3signer/key.key -out web3signer/cert.pem -config web3signer/config &&
-openssl pkcs12 -export -aes256 -out web3signer/key.p12 -inkey web3signer/key.key -in web3signer/cert.pem -password pass:$(cat web3signer/password.txt) &&
+
+# The lighthouse/key_legacy.p12 file is generated specifically for macOS because the default `openssl pkcs12` encoding
+# algorithm in OpenSSL v3 is not compatible with the PKCS algorithm used by the Apple Security Framework. The client
+# side (using the reqwest crate) relies on the Apple Security Framework to parse PKCS files.
+# We don't need to generate web3signer/key_legacy.p12 because the compatibility issue doesn't occur on the web3signer
+# side. It seems that web3signer (Java) uses its own implementation to parse PKCS files.
+# See https://github.com/sigp/lighthouse/issues/6442#issuecomment-2469252651
+
+# We specify `-days 825` when generating the certificate files because Apple requires TLS server certificates to have a
+# validity period of 825 days or fewer.
+# See https://github.com/sigp/lighthouse/issues/6442#issuecomment-2474979183
+
+openssl req -x509 -sha256 -nodes -days 825 -newkey rsa:4096 -keyout web3signer/key.key -out web3signer/cert.pem -config web3signer/config &&
+openssl pkcs12 -export -out web3signer/key.p12 -inkey web3signer/key.key -in web3signer/cert.pem -password pass:$(cat web3signer/password.txt) &&
 cp web3signer/cert.pem lighthouse/web3signer.pem &&
-openssl req -x509 -sha256 -nodes -days 36500 -newkey rsa:4096 -keyout lighthouse/key.key -out lighthouse/cert.pem -config lighthouse/config &&
-openssl pkcs12 -export -aes256 -out lighthouse/key.p12 -inkey lighthouse/key.key -in lighthouse/cert.pem -password pass:$(cat lighthouse/password.txt) &&
+openssl req -x509 -sha256 -nodes -days 825 -newkey rsa:4096 -keyout lighthouse/key.key -out lighthouse/cert.pem -config lighthouse/config &&
+openssl pkcs12 -export -out lighthouse/key.p12 -inkey lighthouse/key.key -in lighthouse/cert.pem -password pass:$(cat lighthouse/password.txt) &&
+openssl pkcs12 -export -legacy -out lighthouse/key_legacy.p12 -inkey lighthouse/key.key -in lighthouse/cert.pem -password pass:$(cat lighthouse/password.txt) &&
 openssl x509 -noout -fingerprint -sha256 -inform pem -in lighthouse/cert.pem | cut -b 20-| sed "s/^/lighthouse /" > web3signer/known_clients.txt
diff --git a/testing/web3signer_tests/tls/lighthouse/cert.pem b/testing/web3signer_tests/tls/lighthouse/cert.pem
index 24b0a2e5c0..4aaf66b747 100644
--- a/testing/web3signer_tests/tls/lighthouse/cert.pem
+++ b/testing/web3signer_tests/tls/lighthouse/cert.pem
@@ -1,33 +1,33 @@
 -----BEGIN CERTIFICATE-----
-MIIFujCCA6KgAwIBAgIUXZijYo8W4/9dAq58ocFEbZDxohwwDQYJKoZIhvcNAQEL
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 -----END CERTIFICATE-----
diff --git a/testing/web3signer_tests/tls/lighthouse/key.key b/testing/web3signer_tests/tls/lighthouse/key.key
index d00b6c2122..2b510c6b6d 100644
--- a/testing/web3signer_tests/tls/lighthouse/key.key
+++ b/testing/web3signer_tests/tls/lighthouse/key.key
@@ -1,52 +1,52 @@
 -----BEGIN PRIVATE KEY-----
-MIIJQgIBADANBgkqhkiG9w0BAQEFAASCCSwwggkoAgEAAoICAQC1R1M9NnRwUsqF
-vJzNWPKuY1PW7llwRRWCixiWNvcxukGTa6AMLZDrYO1Y7qlw5m52aHSA2fs2KyeA
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 -----END PRIVATE KEY-----
diff --git a/testing/web3signer_tests/tls/lighthouse/key.p12 b/testing/web3signer_tests/tls/lighthouse/key.p12
index 73468fa084..f2ef6d20e2 100644
Binary files a/testing/web3signer_tests/tls/lighthouse/key.p12 and b/testing/web3signer_tests/tls/lighthouse/key.p12 differ
diff --git a/testing/web3signer_tests/tls/lighthouse/key_legacy.p12 b/testing/web3signer_tests/tls/lighthouse/key_legacy.p12
new file mode 100644
index 0000000000..c3394fae9a
Binary files /dev/null and b/testing/web3signer_tests/tls/lighthouse/key_legacy.p12 differ
diff --git a/testing/web3signer_tests/tls/lighthouse/web3signer.pem b/testing/web3signer_tests/tls/lighthouse/web3signer.pem
index 6266cadf9b..cae7603320 100644
--- a/testing/web3signer_tests/tls/lighthouse/web3signer.pem
+++ b/testing/web3signer_tests/tls/lighthouse/web3signer.pem
@@ -1,33 +1,33 @@
 -----BEGIN CERTIFICATE-----
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 -----END CERTIFICATE-----
diff --git a/testing/web3signer_tests/tls/web3signer/cert.pem b/testing/web3signer_tests/tls/web3signer/cert.pem
index 6266cadf9b..cae7603320 100644
--- a/testing/web3signer_tests/tls/web3signer/cert.pem
+++ b/testing/web3signer_tests/tls/web3signer/cert.pem
@@ -1,33 +1,33 @@
 -----BEGIN CERTIFICATE-----
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 -----END CERTIFICATE-----
diff --git a/testing/web3signer_tests/tls/web3signer/key.key b/testing/web3signer_tests/tls/web3signer/key.key
index d969753406..97a36d1bb2 100644
--- a/testing/web3signer_tests/tls/web3signer/key.key
+++ b/testing/web3signer_tests/tls/web3signer/key.key
@@ -1,52 +1,52 @@
 -----BEGIN PRIVATE KEY-----
-MIIJQgIBADANBgkqhkiG9w0BAQEFAASCCSwwggkoAgEAAoICAQDScvshqu3747j4
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 -----END PRIVATE KEY-----
diff --git a/testing/web3signer_tests/tls/web3signer/key.p12 b/testing/web3signer_tests/tls/web3signer/key.p12
index 792dc197f8..c6c2da8461 100644
Binary files a/testing/web3signer_tests/tls/web3signer/key.p12 and b/testing/web3signer_tests/tls/web3signer/key.p12 differ
diff --git a/testing/web3signer_tests/tls/web3signer/known_clients.txt b/testing/web3signer_tests/tls/web3signer/known_clients.txt
index c4722fe587..86d61fba75 100644
--- a/testing/web3signer_tests/tls/web3signer/known_clients.txt
+++ b/testing/web3signer_tests/tls/web3signer/known_clients.txt
@@ -1 +1 @@
-lighthouse 02:D0:A8:C0:6A:59:90:40:54:67:D4:BD:AE:5A:D4:F5:14:A9:79:38:98:E0:62:93:C1:77:13:FC:B4:60:65:CE
+lighthouse 49:99:C9:A4:05:4C:EC:BE:FD:0B:C3:C3:C1:2F:A4:D3:AB:70:96:47:51:F5:5B:3B:37:65:31:56:18:B7:B8:AD