With plans to deliver 2443 planes in different versions for the US Air Force, Navy and Marines, the program is now the most expensive in US military history. When it was launched in 2001, however, the one-size-fits-all approach was touted as a way to save money.
"The F-35 was conceived as a relatively affordable fifth-generation strike fighter" that would meet the needs of the Air Force, Navy and Marines with the same airframe instead of having to fund "three separate tactical aircraft designs," according to a Congressional Research Service report.
The cost of Lockheed Martin's Joint Strike Fighter has doubled since 2001 to about $162 million per aircraft, about three times the price of an F-18 Super Hornet fighter.
The total cost of the program is currently estimated at $395.7 billion, according to the Pentagon, a four per cent increase over last year.
"As the program continues to experience cost growth and delays, projected annual funding needs are unprecedented, averaging more than $13 billion a year through 2035," said the Government Accountability Office, the auditing arm of Congress.
The Pentagon maintains that the price of the supersonic, single-engine aircraft over the long term will stay within original plans, once a full rate of production is underway.
"Using today's dollars, the average purchase cost in 2019 will be $81.4 million," said spokesman George Little.
"There have been challenges in the past. We believe we're making progress overtime in putting controls around those overruns."
The program called for launching construction at an early stage, at the same time the aircraft was being put through flight tests -- on the assumption that technical hurdles had been worked out in computer modeling.
The approach was supposed to save time and money, but instead "concurrency" has become a vicious circle. Technical glitches force delays in production schedules, resulting in expensive redesigns and cost overruns.
"Fundamentally, that was a miscalculation," Vice Admiral David Venlet, who was appointed last year to oversee the program, said about concurrency.
Richard Aboulafia, an aerospace analyst with the Teal Group consultancy, said concurrency has had a "huge" impact on cost.
"You start building while you're still testing and while you're testing, you're making design changes, so you have to go back and modify the planes you've already built," he told AFP.
Despite more than five years of delays in the testing program that is due to be completed by 2016, only 20 per cent of the tests have been carried out, raising the prospect of yet more cost overruns.
Tests have revealed a host of problems, including excessive vibration, a malfunctioning high tech helmet display and a flawed tail hook on the F-35C that fails to catch arresting gear wires on aircraft carriers.
There are also persistent software problems, in an aircraft that has 24 million lines of code, three times the number for the latest model US fighter, the F-22 Raptor.
Seeking to reassure Congress, the program's chiefs say the technical challenges amount to growing pains, and that previous aircraft had similar problems.
"All three F-35 variants are encountering the sort of design issues historically encountered in advanced technology programs of this complexity," Venlet and two other senior officials overseeing the program said in a report to Congress in March.
"While the overall F-35 design is sound, there is significant risk remaining in the program."
Given the spate of financial and engineering problems, some experts have questioned the strategic rationale for the F-35, citing the US military's vast fleet of warplanes that outstrips any other air force.
However, the plane's advocates insist the fifth-generation fighter is needed to penetrate enemy radar undetected and swiftly deliver a blow to a potential adversary, usually portrayed as China.
After the attacks of September 11, 2001, the F-35 project was shaped by an era of abundance for the Pentagon, which former Defense Secretary Robert Gates castigated as "a culture of endless spending."
That time has passed. To limit the damage, the Defense Department expects to build 365 planes by 2017, instead of an initial plan for 1,591 in the same period. The difference would be made up later on, when technical problems are supposed to be solved.
Air Force Secretary Michael Donley has made clear there are no additional funds available if there are more cost overruns.
"We'll have to take down the number of aircraft that we have planned in procurement to pay for that work, because no more money is going to be migrating into this program."