The contract to build John Adams was awarded to Portsmouth Naval Shipyard in Kittery, Maine, on 23 July 1960 and her keel was laid down there on 19 May 1961.

Following her commissioning, John Adams completed sixteen deterrent patrols while assigned to the United States Atlantic Fleet After her sixteenth patrol, she entered Puget Sound Naval Shipyard in Bremerton, Washington for overhaul and modernization in August 1968.

Upon completion of her thirty-second deterrent patrol, John Adams entered Portsmouth Naval Shipyard at Kittery for her second overhaul and conversion to the Poseidon missile system.

After completing an additional forty-three deterrent patrols from both her home port at Charleston, South Carolina, and from Holy Loch, Scotland, John Adams transited the Panama Canal to again enter the Puget Sound Navy Shipyard, this time in preparation for decommissioning after a long and distinguished career.

John Adams was decommissioned on 24 March 1989 and stricken from the Naval Vessel Register the same day.