President Mahmoud Ahmadinejad, before a crowd of Iranian military officials including the country's defense minister and the Armed Forces chief of staff, presided over a ceremony trumpeting the Jamaran-2's indigenous design, "state-of-the-art" navigation equipment and "complex" defensive systems.
Iranian state media admitted the ship has not yet completed final testing.
The ship weighs 1,420 tons and is powered by a 20,000-horsepower engine, which could take it to a speed of 30 knots, the official release stated. It is reportedly capable of carrying helicopters, surface-to-surface and surface-to-air missiles, artillery and torpedoes.
"The destroyer is a symbol of the Islamic Republic's capability and strength and conveys the message of peace and friendship to the Caspian Sea states," read the official statement.
Over two decades, Iran has worked to build a self-sufficient military supported by equipment produced wholly in-country, to mixed results.
While it was able to successfully launch a predecessor to the Jamaran-2 into the Persian Gulf in 2010, the unveiling of a "super stealth" jet in February was met with derision on the world stage when it appeared to be incapable of flight.
And in January, Iran's fledgling space program claimed to safely send a monkey into suborbital flight, although photos showing the animal before and after the launch raised suspicions that the venture had failed and it had died or disappeared.
Ahmadinejad said he would be willing to volunteer to be the first human to participate in a manned flight by Iran's space program.