diff --git a/barretenberg/cpp/src/barretenberg/api/api_chonk.cpp b/barretenberg/cpp/src/barretenberg/api/api_chonk.cpp
index bb0d8080c168..9c290315fff1 100644
--- a/barretenberg/cpp/src/barretenberg/api/api_chonk.cpp
+++ b/barretenberg/cpp/src/barretenberg/api/api_chonk.cpp
@@ -123,7 +123,7 @@ bool ChonkAPI::verify([[maybe_unused]] const Flags& flags,
     auto proof_fields = many_from_buffer<fr>(read_file(proof_path));
     auto proof = ChonkProof::from_field_elements(proof_fields);
 
-    auto vk_buffer = read_file(vk_path);
+    auto vk_buffer = read_vk_file(vk_path);
 
     auto response = bbapi::ChonkVerify{ .proof = std::move(proof), .vk = std::move(vk_buffer) }.execute();
     return response.valid;
diff --git a/barretenberg/cpp/src/barretenberg/api/api_ultra_honk.cpp b/barretenberg/cpp/src/barretenberg/api/api_ultra_honk.cpp
index b7e335b6237c..0d7f08e947a6 100644
--- a/barretenberg/cpp/src/barretenberg/api/api_ultra_honk.cpp
+++ b/barretenberg/cpp/src/barretenberg/api/api_ultra_honk.cpp
@@ -101,7 +101,7 @@ bool UltraHonkAPI::verify(const Flags& flags,
     // Read input files
     auto public_inputs = many_from_buffer<uint256_t>(read_file(public_inputs_path));
     auto proof = many_from_buffer<uint256_t>(read_file(proof_path));
-    auto vk_bytes = read_file(vk_path);
+    auto vk_bytes = read_vk_file(vk_path);
 
     // Convert flags to ProofSystemSettings
     bbapi::ProofSystemSettings settings{ .ipa_accumulation = flags.ipa_accumulation,
@@ -209,7 +209,7 @@ void UltraHonkAPI::write_solidity_verifier(const Flags& flags,
 {
     BB_BENCH_NAME("UltraHonkAPI::write_solidity_verifier");
     // Read VK file
-    auto vk_bytes = read_file(vk_path);
+    auto vk_bytes = read_vk_file(vk_path);
 
     // Convert flags to ProofSystemSettings
     bbapi::ProofSystemSettings settings{ .ipa_accumulation = flags.ipa_accumulation,
diff --git a/barretenberg/cpp/src/barretenberg/api/api_ultra_honk.test.cpp b/barretenberg/cpp/src/barretenberg/api/api_ultra_honk.test.cpp
index b84d75c2efbc..93e9424154ba 100644
--- a/barretenberg/cpp/src/barretenberg/api/api_ultra_honk.test.cpp
+++ b/barretenberg/cpp/src/barretenberg/api/api_ultra_honk.test.cpp
@@ -233,3 +233,35 @@ TEST_F(ApiUltraHonkTest, GatesWithOpcodesSmokeTest)
     // Check that output contains per-opcode information
     EXPECT_TRUE(output.find("gates_per_opcode") != std::string::npos);
 }
+
+TEST_F(ApiUltraHonkTest, VerifyWithMissingVkGivesActionableError)
+{
+    auto [bytecode_path, witness_path] = create_test_circuit_files(test_dir);
+
+    API::Flags flags;
+    flags.oracle_hash_type = "poseidon2";
+    flags.write_vk = true;
+
+    UltraHonkAPI api;
+
+    // Generate proof with vk
+    auto proof_output_dir = test_dir / "proof";
+    std::filesystem::create_directories(proof_output_dir);
+    api.prove(flags, bytecode_path, witness_path, "", proof_output_dir);
+
+    // Try to verify with a non-existent vk path
+    auto nonexistent_vk_path = test_dir / "nonexistent_vk";
+    try {
+        api.verify(flags, proof_output_dir / "public_inputs", proof_output_dir / "proof", nonexistent_vk_path);
+        FAIL() << "Expected an exception to be thrown";
+    } catch (const std::runtime_error& e) {
+        std::string error_msg = e.what();
+        // Check that the error message contains actionable guidance
+        EXPECT_TRUE(error_msg.find("--write_vk") != std::string::npos)
+            << "Error message should mention --write_vk flag. Got: " << error_msg;
+        EXPECT_TRUE(error_msg.find("bb write_vk") != std::string::npos)
+            << "Error message should mention bb write_vk command. Got: " << error_msg;
+        EXPECT_TRUE(error_msg.find("--vk_path") != std::string::npos)
+            << "Error message should mention --vk_path option. Got: " << error_msg;
+    }
+}
diff --git a/barretenberg/cpp/src/barretenberg/api/file_io.hpp b/barretenberg/cpp/src/barretenberg/api/file_io.hpp
index c5436170d0ca..fe9cf30adf5f 100644
--- a/barretenberg/cpp/src/barretenberg/api/file_io.hpp
+++ b/barretenberg/cpp/src/barretenberg/api/file_io.hpp
@@ -5,6 +5,7 @@
 #include <cstdint>
 #include <cstring>
 #include <fcntl.h>
+#include <filesystem>
 #include <fstream>
 #include <ios>
 #include <iostream>
@@ -100,4 +101,23 @@ template <typename Fr> inline std::string field_elements_to_json(const std::vect
     ss << "]";
     return ss.str();
 }
+
+/**
+ * @brief Read a verification key file with an actionable error message if not found.
+ *
+ * @param vk_path Path to the verification key file
+ * @return std::vector<uint8_t> The verification key bytes
+ * @throws std::runtime_error with actionable message if vk file not found
+ */
+inline std::vector<uint8_t> read_vk_file(const std::filesystem::path& vk_path)
+{
+    try {
+        return read_file(vk_path);
+    } catch (const std::runtime_error&) {
+        THROW std::runtime_error("Unable to open file: " + vk_path.string() +
+                                 "\nGenerate a vk during proving by running `bb prove` with an additional `--write_vk` "
+                                 "flag, or run `bb write_vk` to generate a standalone vk."
+                                 "\nIf you already have a vk file, specify its path with `--vk_path <path>`.");
+    }
+}
 } // namespace bb