The F-35C carrier variant features larger wings with foldable wingtip sections, larger wing and tail control surfaces for improved low-speed control, stronger landing gear for the stresses of carrier arrested landings, a twin-wheel nose gear, and a stronger tailhook for use with carrier arrestor cables. The larger wing area allows for decreased landing speed while increasing both range and payload. With twice the range on internal fuel as the F/A-18C Hornet, the F-35C achieves much the same goal as the F/A-18E/F Super Hornet.

The United States Navy will use the F-35C carrier variant. It intends to buy 480 F-35Cs to replace the F/A-18A, B, C, and D Hornets. The F-35C will also serve as a low-observable complement to the Super Hornet. On 27 June 2007, the carrier variant completed its Air System Critical Design Review (CDR). This allows the first two functional prototype F-35C units to be produced. The C variant is expected to be available beginning in 2014. The first F-35C was rolled out on 29 July 2009. On 6 November 2010, the first F-35C arrived at Naval Air Station Patuxent River, however, it was determined that the replacement engines for at-sea repair are too large to be transported by current underway replenishment systems. The Marine Corps will also purchase 80 F-35Cs, enough for five squadrons, for use with Navy carrier air wings in a joint service agreement signed on 14 March 2011.

In October 2010, the United Kingdom decided to change its F-35B order to the F-35C, which will be used for both land and naval operations.[262] The total number of F-35C aircraft to be procured has not been announced. However, it will be less than the 150 originally planned. The Royal Navy’s new Queen Elizabeth class aircraft carriers are large enough to support non-STOVL operations and as a result, at least HMS Queen Elizabeth will have catapults and arrestor cables installed to allow F-35C and Allied naval aircraft operations.[244][262] The carrier will typically carry 12 F-35Cs with the ability to deploy up to 36. The UK Strategic Defence & Security Review found that the F-35C’s greater endurance in the air meant that fewer aircraft would be needed and that the F-35C has a 25 percent lower lifetime cost than the F-35B.

In 2011 the F-35Cs were grounded for six days because of a software error in the code that was intended to keep the wings from folding in mid-flight.

On 27 July 2011, the F-35C test aircraft CF-3 completed its first steam catapult launch during a test flight in Naval Air Engineering Station Lakehurst. The TC-13 Mod 2 test steam catapult, representative of current fleet technology, was used. In addition to the catapult launches at varying power levels, the integrated test team is to execute a test plan over three weeks to include dual-aircraft jet blast deflector testing and catapult launches using a degraded catapult configuration to measure the effects of steam ingestion on the aircraft.