Gilmer's final political office was as the 15th Secretary of the Navy, but he died in an accident ten days after assuming that position.

He was taught by private tutors and his uncle Peachy Ridgeway Gilmer in Charlottesville and Staunton, and studied law in Liberty (now Bedford), Virginia.

While in office, he disagreed with the Virginia General Assembly over the extradition of slave stealers, which played a part in his running for Congress the following winter.

On February 15, 1844, he was appointed by Tyler to be the U.S. Secretary of the Navy, and resigned his seat in the Congress the next day to enter on the duties of the office; but, ten days later, he was killed by the bursting of a bow gun on board USS Princeton while on a tour of the Potomac River below Washington.

His death meant the loss of a valuable ally for Tyler, and some historians suggest that it may have delayed the Texas Annexation effort.