The contract to build Carter was awarded to the Electric Boat Division of General Dynamics Corporation in Groton, Connecticut on 29 June 1996 and her keel was laid down on 5 December 1995. Original schedules called for Carter to be commissioned in late 2001 or early 2002, but on 10 December 1999 Electric Boat was awarded an US$887 million extension to the Carter contract to modify the boat for highly classified missions and testing of new submarine systems. Once in service, Carter will relieve Parche (SSN-683) in performing these types of missions.

Carter is roughly 100 feet longer than the other two ships of her class. This is due to the insertion of a section known as the Multi-Mission Platform (MMP), which allows launch and recovery of ROVs and Navy SEAL forces. The plug features a fairing over a wasp-waist shaped passageway allowing crew to pass between the fore and aft sections of the hull while providing a space to store ROVs and special equipment that may need to launch and recover from the submarine.

In addition, additional maneuvering devices are fitted fore and aft that will allow her to keep station over selected targets in odd currents. Past submarines that were so outfitted were used to place listening devices on undersea cables and listen on communications of foreign countries.