Cuttlefish was the first submarine built at EB's facility in Groton, Connecticut; construction of previous Electric Boat designs had been subcontracted to other shipyards, notably Fore River Shipbuilding of Quincy, Massachusetts.

Due to pressure from the Submarine Officers Conference,[5] they featured full double hulls derived from the concept of the Kaiserliche Marine's U-135,[5] direct-drive diesel propulsion systems, a separate crew's mess (reinstated thanks to EB's rearrangement of the internal layout; Portsmouth would follow soon after),[5] and considerable space around the conning tower within the large bridge fairwater (which was drastically cut down in World War II when the 3-inch (76 mm) deck gun was relocated forward of the bridge).

Portsmouth, while welding non-critical areas on Cachalot like the superstructure, piping brackets, support framing and interior tanks, continued to use riveting for both the inner and outer hulls.

[2] The auxiliary engine was for charging batteries or for increased surface speed via a diesel-electric system providing power to the main electric motors.

Due to the full double hull design, the external tanks proved too narrow for easy maintenance,[11] and the MAN diesels were a constant headache, demanding re-engining[11] with General Motors-Winton four-cycle 16-258 engines in 1936-38.