diff --git a/fuzz/Cargo.toml b/fuzz/Cargo.toml
index db35b00bae..194b1046c9 100644
--- a/fuzz/Cargo.toml
+++ b/fuzz/Cargo.toml
@@ -17,6 +17,7 @@ cargo-fuzz = true
 libfuzzer-sys = "0.4.10"
 arbitrary = { version = "1.4.2", features = ["derive"] }
 binary_sv2 = { path = "../sv2/binary-sv2"}
+noise_sv2 = { path = "../sv2/noise-sv2" }
 parsers_sv2 = { path = "../sv2/parsers-sv2" }
 framing_sv2 = { path = "../sv2/framing-sv2" }
 codec_sv2 = { path = "../sv2/codec-sv2", features = ["noise_sv2"]}
@@ -24,6 +25,8 @@ common_messages_sv2 = { path = "../sv2/subprotocols/common-messages" }
 job_declaration_sv2 = { path = "../sv2/subprotocols/job-declaration" }
 mining_sv2 = {path = "../sv2/subprotocols/mining" }
 template_distribution_sv2 = { path = "../sv2/subprotocols/template-distribution" }
+secp256k1 = { version = "0.28.2", default-features = false, features = ["alloc", "rand"] }
+rand = { version = "0.8.5", default-features = false }
 
 [[bin]]
 name = "deserialize_sv2frame"
@@ -67,3 +70,8 @@ path = "fuzz_targets/end_to_end_serialization_for_datatypes.rs"
 test = false
 doc = false
 
+[[bin]]
+name = "fuzz_noise_handshake_and_roundtrip_encryption"
+path = "fuzz_targets/fuzz_noise_handshake_and_roundtrip_encryption.rs"
+test = false
+doc = false
diff --git a/fuzz/fuzz_targets/fuzz_noise_handshake_and_roundtrip_encryption.rs b/fuzz/fuzz_targets/fuzz_noise_handshake_and_roundtrip_encryption.rs
new file mode 100644
index 0000000000..d50ccabadc
--- /dev/null
+++ b/fuzz/fuzz_targets/fuzz_noise_handshake_and_roundtrip_encryption.rs
@@ -0,0 +1,186 @@
+#![no_main]
+
+use arbitrary::Arbitrary;
+use libfuzzer_sys::fuzz_target;
+use noise_sv2::{Initiator, Responder};
+use secp256k1::{Keypair, Secp256k1, XOnlyPublicKey};
+
+use rand::{rngs::StdRng, SeedableRng};
+
+// Generates a secp256k1 keypair from a given random seed.
+// Used to create deterministic keys for both initiator and responder during fuzzing.
+//
+// Per specification 4.3.1.1: No assumption is made about the parity of Y-coordinate.
+// For signing (certificate) and ECDH (handshake) it is not necessary to "grind" the private key.
+// see: https://github.com/stratum-mining/sv2-spec/blob/161f21cf2c618327b6c929ee0cf706e85a59f6d9/04-Protocol-Security.md?plain=1#L67
+fn generate_key(rand_seed: u64) -> Keypair {
+    let secp = Secp256k1::new();
+    let mut rng = StdRng::seed_from_u64(rand_seed);
+
+    let (secret_key, _public_key) = secp.generate_keypair(&mut rng);
+
+    Keypair::from_secret_key(&secp, &secret_key)
+}
+
+// Represents the relationship between the initiator and responder during the Noise handshake.
+// This determines whether the initiator knows and trusts the responder's public key.
+#[derive(PartialEq, Arbitrary, Debug)]
+enum PeerMode {
+    // Initiator does not know the responder's public key -> performs anonymous handshake
+    Unknown,
+    // Initiator knows and expects the responder's specific public key -> authenticated handshake
+    Known,
+    // Initiator knows a different peer's key (not the responder's) -> handshake should fail
+    PeerDifferentFromResponder,
+}
+
+// Input structure for the fuzzer, containing all parameters to control the test.
+// Generated by the arbitrary crate from raw fuzz input bytes.
+#[derive(Debug, Arbitrary)]
+struct FuzzInput {
+    // Controls whether initiator knows responder's public key
+    peer_mode: PeerMode,
+    // Certificate validity duration in seconds (passed to responder)
+    cert_validity: u32,
+    // Message payload to encrypt and decrypt (fuzzed data)
+    message: Vec<u8>,
+    // Whether to corrupt message/handshake with bit flips
+    should_corrupt_message: bool,
+    // Index into the message/handshake where corruption occurs
+    corruption_index: usize,
+    // Seed for generating cryptographic keys
+    rand_seed: u64,
+}
+
+// Corrupts a message by XORing a byte at the specified index with 0xFF.
+// This simulates bit-flipping noise on the wire, testing error handling.
+//
+// # Arguments
+// * `should_corrupt` - If true, performs the corruption
+// * `corruption_index` - Index of byte to flip (wrapped via modulo)
+// * `message` - Mutable slice to corrupt in-place
+fn maybe_corrupt_message(should_corrupt: bool, corruption_index: usize, message: &mut [u8]) {
+    if should_corrupt && !message.is_empty() {
+        let index = corruption_index % message.len();
+        message[index] ^= 0xFF;
+    }
+}
+
+// Main fuzz target that tests the Noise protocol handshake and encrypted message roundtrip.
+//
+// This fuzzer exercises:
+// 1. Full Noise handshake between initiator and responder
+// 2. Encryption of messages after successful handshake
+// 3. Decryption of messages by the receiver
+// 4. Error handling for corrupted data and mismatched peers
+//
+// The fuzzer validates both success cases (valid handshake + clean message)
+// and failure cases (corrupted messages should fail, wrong peer should fail).
+fuzz_target!(|input: FuzzInput| {
+    let mut secret_message = input.message.clone();
+
+    // Generate the responder's keypair from the fuzzed seed
+    let responder_kp = generate_key(input.rand_seed);
+    let responder_pk: XOnlyPublicKey = responder_kp.public_key().x_only_public_key().0;
+
+    // Determine if the initiator knows the responder's key
+    // This affects the Noise handshake pattern (anonymous vs authenticated)
+    let known_peer = match input.peer_mode {
+        // Initiator has no prior knowledge of responder -> performs anonymous handshake
+        PeerMode::Unknown => None,
+        // Initiator knows responder's exact public key -> authenticated handshake
+        PeerMode::Known => Some(responder_pk),
+        // Initiator knows a DIFFERENT peer's key -> handshake should fail
+        PeerMode::PeerDifferentFromResponder => Some(
+            generate_key(input.rand_seed ^ 0xcafe_babe)
+                .public_key()
+                .x_only_public_key()
+                .0,
+        ),
+    };
+
+    // Create initiator (client) - optionally knows the responder
+    let mut initiator = Initiator::new(known_peer);
+
+    // Create responder (server) with the generated keypair and certificate validity
+    let mut responder = Responder::new(responder_kp, input.cert_validity);
+
+    // ========== Handshake Phase ==========
+
+    // Step 0: Initiator creates its first handshake message
+    let first_message = initiator
+        .step_0()
+        .expect("Initiator failed first step of handshake");
+
+    // Step 1: Responder processes initiator's message and creates response
+    let (mut second_message, mut responder_state) = responder
+        .step_1(first_message)
+        .expect("Responder failed second step of handshake");
+
+    // Optionally corrupt the responder's handshake message to test error handling
+    maybe_corrupt_message(
+        input.should_corrupt_message,
+        input.corruption_index,
+        &mut second_message,
+    );
+
+    // Step 2: Initiator processes responder's message, completing the handshake
+    // This returns the encrypted session state on success
+    let mut initiator_state = match initiator.step_2(second_message) {
+        Ok(state) => {
+            // If we used a different peer key, handshake should have failed
+            if input.peer_mode == PeerMode::PeerDifferentFromResponder {
+                panic!(
+                    "Initiator should have failed handshake with a peer different from responder"
+                );
+            }
+            state
+        }
+        Err(e) => {
+            // If we didn't use a wrong peer AND didn't corrupt, handshake should succeed
+            if input.peer_mode != PeerMode::PeerDifferentFromResponder
+                && !input.should_corrupt_message
+            {
+                panic!("Initiator should have succeeded handshake with known peer: {e:?}");
+            }
+            return;
+        }
+    };
+
+    // ========== Encrypted Message Phase ==========
+
+    // Initiator encrypts the message using the established session
+    initiator_state
+        .encrypt(&mut secret_message)
+        .expect("Initiator failed to encrypt message");
+
+    // Optionally corrupt the encrypted message to test decryption failure handling
+    maybe_corrupt_message(
+        input.should_corrupt_message,
+        input.corruption_index,
+        &mut secret_message,
+    );
+
+    // Responder attempts to decrypt the message
+    match responder_state.decrypt(&mut secret_message) {
+        Ok(()) => {
+            // If we corrupted the message, decryption should have failed
+            if input.should_corrupt_message {
+                panic!("Responder should have failed to decrypt corrupted message");
+            }
+        }
+        Err(e) => {
+            // If message wasn't corrupted, decryption should succeed
+            if !input.should_corrupt_message {
+                panic!("Responder should have succeeded to decrypt uncorrupted message: {e:?}");
+            }
+            return;
+        }
+    }
+
+    // Verify the decrypted message matches the original
+    assert_eq!(
+        input.message, secret_message,
+        "Decrypted message does not match original"
+    );
+});