The contract to build Darter was awarded to the Electric Boat Division of General Dynamics Corporation in Groton, Connecticut on 30 June 1954 and her keel was laid down on 10 November 1954.

Designed under project SCB 116[1] with sophisticated acoustic, electronic and fire control gear, Darter was intended to serve as a new generation of post-war ASW submarines, similar to USS Tang (SS-563).

Following an overhaul at Portsmouth Naval Shipyard she changed homeport to Charleston, South Carolina on 1 August 1959 and began training missions in support of the newly commissioned fleet ballistic missile submarines, providing anti-submarine warfare (ASW) services for surface units in the West Indies and off Key West, Florida, and serving as a platform for various Chief of Naval Operations (CNO) projects.

She also received a major modernization overhaul at Charleston Naval Shipyard in 1965, receiving a 16-foot (5 m) hull extension (the "plug", just forward of the engine room), new engines, new safety gear (SUBSAFE), better electronic gear (including the AN/BQG-4 Passive Underwater Fire Control Feasibility System (PUFFS) passive sonar with three shark-fin domes added topside) and other upgrades.

Shifting homeports again in 1971, she moved to San Diego, California, Darter made four Western Pacific (WestPac) deployments in support of 7th Fleet operations.