The car debuted with a factory suggested retail price of approximately US$400,000, although some buyers were reported to have paid as much as US$1.6 million. A total of 1,315 F40s were produced.
Ostensibly, the F40 was conceived as the successor to the 288 GTO and designed to compete with vehicles such as the Porsche 959 and Lamborghini Countach; for Ferrari management, the vehicle was a major statement piece. Over a period of several years prior to the F40's conception, the company's dominance in racing had waned significantly, and even in Formula One, an arena they had once dominated, victories had become sparse. Enzo Ferrari had recently turned 90 years old, and was keenly aware that time was not on his side. He wanted his new sports car to serve as his final statement-maker, a vehicle encompassing the best in track-developed technology and capable of being a showcase for what the Ferrari engineers were capable of creating. The company's upcoming 40th anniversary provided just the right occasion for the car to debut.
As Enzo had predicted it would be, the F40 was the last car to be commissioned by him before his death.
As early as 1984, the Maranello factory had begun development of an evolution model of the 288 GTO intended to compete against the Porsche 959 in FIA Group B. However, when the FIA brought an end to the Group B category for the 1986 season, Enzo was left with five 288 GTO Evoluzione development cars, and no series in which to campaign them. Enzo's desire to leave a legacy in his final supercar allowed the Evoluzione program to be further developed to produce a car exclusively for road use.
Power came from an enlarged, 2.9 L (2936 cc) version of the GTO's twin IHI turbocharged V8 developing 478 PS (352 kW; 471 hp) under 110 kPa (16 psi) of boost. The F40 did without a catalytic converter until 1990 when US regulations made them a requirement for emissions control reasons. The flanking exhaust pipes guide exhaust gases from each bank of cylinders while the central pipe guides gases released from the wastegate of the turbochargers.
The suspension setup was similar to the GTO's double wishbone setup, though many parts were upgraded and settings were changed; the unusually low ground clearance prompted Ferrari to include the ability to raise the vehicle's ground clearance when necessary.
The body was an entirely new design by Pininfarina featuring panels made of kevlar, carbon fiber, and aluminum for strength and low weight, and intense aerodynamic testing was employed (see below). Weight was further minimized through the use of a plastic windshield and windows. Although the cars did have air conditioning, no carpets, sound system, or door handles were installed. The first 50 cars produced had sliding Lexan windows, while later cars were fitted with normal windows that could be rolled down.
The F40 was designed with aerodynamics in mind. For speed the car relied more on its shape than its power. Frontal area was reduced, and airflow greatly smoothed, but stability rather than terminal velocity was a primary concern. So too was cooling as the forced induction engine generated a great deal of heat. In consequence, the car was somewhat like an open-wheel racing car with a body. It had a partial undertray to smooth airflow beneath the radiator, front section, and the cabin, and a second one with diffusers behind the motor, but the engine bay was not sealed. Nonetheless, the F40 had an impressively low Cd of 0.34 with lift controlled by its spoilers and wing.
The factory never intended to race the F40, but the car saw competition as early as 1989 when it debuted in the Laguna Seca round of the IMSA, appearing in the GTO category, with a LM evolution model driven by Jean Alesi, finishing third to the two faster spaceframed four wheel drive Audi 90 and beating a host of other factory backed spaceframe specials that dominated the races. Despite lack of factory backing, the car would soon have another successful season there under a host of guest drivers such as Jean-Pierre Jabouille, Jacques Laffite and Hurley Haywood taking a total of three second places and one third.
Although the F40 would not return to IMSA for the following season, it would later be a popular choice by privateers to compete in numerous domestic GT series including JGTC. In 1994, the car made its debut in international competitions, with one cars campaigned in the BPR Global GT Series by Strandell, winning at the 4 Hours of Vallelunga. In 1995, the number of F40s climbed to four, developed independently by Pilot-Aldix Racing (F40 LM) and Strandell (F40 GTE, racing under the Ferrari Club Italia banner), winning the 4 Hours of Anderstorp. No longer competitive against the McLaren F1 GTR, the Ferrari F40 returned for another year in 1996, managing to repeat the previous year's Anderstorp win, and from then on it was no longer seen in GT racing.
The F40 was discontinued in 1992 and in 1995 was intended to be succeeded by the F50 in GT1 racing but only three racing F50s were produced and none ever actually competed in a race.
The F40's light weight of 1,100 kg (2,425 lb) and high power output of 478 PS (352 kW; 471 hp) at 7000 rpm gave the vehicle tremendous performance potential. Road tests have produced 0–100 km/h (0–62 mph) times as low as 3.8 seconds (while the track only version came in at 3.2 seconds), with 0–160 km/h (0–99 mph) in 7.6 seconds and 0–200 km/h (0–120 mph) in 11 seconds giving the F40 a slight advantage in acceleration over the Porsche 959, its primary competitor at the time.
The F40 was the first road legal production car to break the 200 mph (320 km/h) barrier. From its introduction in 1987 until 1989 its only competitors were the Porsche 959 and the 1988 Lamborghini Countach (it was later overtaken by the Lamborghini Diablo), it held the record as the world's fastest production car, with a top speed of 200 mph (320 km/h). During the 2006 Bonneville Speed Week, Amir Rosenbaum of Spectre Performance managed to take his F40 with small boost and air intake modifications to 226 miles per hour (364 km/h).