The aircraft descends from the Lockheed Martin X-35, which in 2001 beat the Boeing X-32 to win the Joint Strike Fighter (JSF) program intended to replace the F-16 Fighting Falcon, F/A-18 Hornet, and the McDonnell Douglas AV-8B Harrier II "jump jet", among others.

Amid increased budget pressure, the DoD's Bottom-Up Review (BUR) in September 1993 announced MRF's and A/F-X's cancellations, with applicable experience brought to the emerging JAST program.

[19] JAST was subsequently renamed to Joint Strike Fighter (JSF) in 1995, with STOVL submissions by McDonnell Douglas, Northrop Grumman, Lockheed Martin,[N 2] and Boeing.

The JSF was expected to eventually replace large numbers of multi-role and strike fighters in the inventories of the US and its allies, including the Harrier, F-16, F/A-18, Fairchild A-10 Thunderbolt II, and Lockheed F-117 Nighthawk.

The key aspect of the X-35 that enabled STOVL operation, the SDLF system consists of the lift fan in the forward center fuselage that could be activated by engaging a clutch that connects the driveshaft to the turbines and thus augmenting the thrust from the engine's swivel nozzle.

The F-35B gained the most, largely due to a 2003 decision to enlarge the weapons bays for commonality between variants; the total weight growth was reportedly up to 2,200 pounds (1,000 kg), over 8%, causing all STOVL key performance parameter (KPP) thresholds to be missed.

[83] The three tiers of international participation generally reflect financial stake in the program, the amount of technology transfer and subcontracts open for bid by national companies, and the order in which countries can obtain production aircraft.

Flight control surfaces include leading-edge flaps, flaperons,[N 11] rudders, and all-moving horizontal tails (stabilators); leading edge root extensions or chines[97] also run forwards to the inlets.

The relatively short 35-foot wingspan of the F-35A and F-35B is set by the requirement to fit inside USN amphibious assault ship parking areas and elevators; the F-35C's larger wing is more fuel efficient.

[123] The ASQ-239 Barracuda electronic warfare system has ten radio frequency antennas embedded into the edges of the wing and tail for all-aspect radar warning receiver (RWR).

It also provides sensor fusion of radio frequency and infrared tracking functions, geolocation threat targeting, and multispectral image countermeasures for self-defense against missiles.

[124] The AAQ-40 EOTS is mounted behind a faceted low-observable window under the nose and performs laser targeting, forward-looking infrared (FLIR), and long range IRST functions.

Instead of the head-up display mounted atop the dashboard of earlier fighters, the HMDS puts flight and combat information on the helmet visor, allowing the pilot to see it no matter which way they are facing.

[166][167] In 2016, the Gen 3 helmet with improved night vision camera, new liquid crystal displays, automated alignment and software enhancements was introduced with LRIP lot 7.

[195] The USAF plans for the F-35A to take up the close air support (CAS) mission in contested environments; amid criticism that it is not as well suited as a dedicated attack platform, USAF chief of staff Mark Welsh placed a focus on weapons for CAS sorties, including guided rockets, fragmentation rockets that shatter into individual projectiles before impact, and more compact ammunition for higher capacity gun pods.

Derived from the Pratt & Whitney F119 used by the F-22, the F135 has a larger fan and higher bypass ratio to increase subsonic thrust and fuel efficiency, and unlike the F119, is not optimized for supercruise.

The thrust vectoring 3BSM nozzle allows the main engine exhaust to be deflected downward at the tail of the aircraft and is moved by a "fueldraulic" actuator that uses pressurized fuel as the working fluid.

Using technology from the General Electric YF120, the F136 was claimed to have a greater temperature margin than the F135 due to the higher mass flow design making full use of the inlet.

[224] Due to numerous problems,[225] such as unreliable diagnoses, excessive connectivity requirements, and security vulnerabilities, ALIS is being replaced by the cloud-based Operational Data Integrated Network (ODIN).

[N 15][244][245] Early flight control laws had problems with "wing drop"[N 16] and also made the airplane sluggish, with high angles-of-attack tests in 2015 against an F-16 showing a lack of energy.

[252] After the redesigned tail hook arrived, the F-35C's carrier-based Development Test I began in November 2014 aboard USS Nimitz and focused on basic day carrier operations and establishing launch and recovery handling procedures.

[260][261][262] During the Low Rate Initial Production (LRIP) phase, the three U.S. military services jointly developed tactics and procedures using flight simulators, testing effectiveness, discovering problems and refining design.

[274] In addition to deploying F-35Bs on amphibious assault ships, the USMC plans to disperse the aircraft among austere forward-deployed bases with shelter and concealment to enhance survivability while remaining close to a battlespace.

[276] The first USMC F-35C squadron, VMFA-314, achieved Full Operational Capability in July 2021 and was first deployed on board USS Abraham Lincoln as a part of Carrier Air Wing 9 in January 2022.

[3] F-35As conducted their first Red Flag exercise in 2017; system maturity had improved and the aircraft scored a kill ratio of 15:1 against an F-16 aggressor squadron in a high-threat environment.

[325][326][327] On 2 November 2023, the IDF posted on social media that they used an F-35I to shoot down a Houthi cruise missile over the Red Sea that was fired from Yemen during the Israel-Hamas War.

Commander of the Royal Norwegian Air Force, Major General Rolf Folland, said: "Fighter jets are vulnerable on the ground, so by being able to use small airfields – and now motorways – (this) increases our survivability in war,"[336] On 27 December 2021, the Netherlands declared initial operational capability (IOC) for its fleet of 24 F-35As that it has received to date from its order for 46 F-35As.

The main computer has a plug-and-play function for add-on systems; proposals include an external jamming pod, and new Israeli air-to-air missiles and guided bombs in the internal weapon bays.

[357] One alternative proposal would have been the adoption of the F-35C for its probe refueling and lower landing speed; however, the Parliamentary Budget Officer's report cited the F-35C's limited performance and payload as being too high a price to pay.

[358] Following the 2015 Federal Election the Liberal Party, whose campaign had included a pledge to cancel the F-35 procurement,[359] formed a new government and commenced an open competition to replace the existing CF-18 Hornet.