Ferrari developed the 335 S as a direct response to the Maserati 450S. The 4.5-litre Maserati engine threatened to overpower Ferrari’s existing 3.8-litre 315 S and 3.5-litre 290 MM models. The 335 S was an evolution of the 315 S, utilizing an upgraded version of the Jano V12 engine.
The engine featured a displacement of 4,023.32 cc (4.0 L) and produced a maximum power output of 400 PS (395 hp; 294 kW) at 7,400 rpm. This power increase allowed the car to reach an estimated top speed of approximately 300 km/h (186 mph). Of the four cars produced, the first two (0674 and 0676) were originally 315 S models that were later converted to 335 S specifications.
The 335 S made its World Championship debut during the third round of the 1957 season at the Mille Miglia. The race proved disastrous for the model and the event itself. Driver Alfonso de Portago, substituting for an ill Luigi Musso, was running in third place in car #531 (chassis 0676) on a straight sector between Cerlongo and Guidizzolo when a tyre exploded. The car struck a telephone pole, crossed a brook, and hit several spectators before bouncing back onto the road and landing in another brook. The accident killed de Portago, his navigator Edmund Gunner Nelson, and nine spectators. The car was destroyed, and the public outrage following the crash led to the permanent cancellation of the Mille Miglia after 1957.
In the same race, the 335 S driven by Peter Collins and Louis Klemantaski (chassis 0700) broke down while leading, which allowed a Ferrari 315 S driven by Piero Taruffi to take the victory.
Following the Mille Miglia, Ferrari entered chassis 0700 for Peter Collins and Olivier Gendebien at the Nürburgring 1000km, where they finished second behind an Aston Martin DBR1. At the 24 Hours of Le Mans, the 335 S models failed to finish, resulting in a 1-2-3-4 sweep for the Jaguar D-Types. However, the 335 S (0700) driven by Collins and Phil Hill secured second place at the Swedish GP, while Mike Hawthorn and Luigi Musso finished fourth in chassis 0674.
The model achieved its primary success in the final round of the World Sports Car Championship at the Venezuelan Grand Prix. Collins and Hill won the race in chassis 0700, followed by Hawthorn and Musso in second place in chassis 0674. These points, combined with earlier season wins by the 315 S and 290 MM, secured the World title for Ferrari.
The 335 S also competed in non-championship events. Olivier Gendebien drove chassis 0700 to a third-place finish at the Grand Prix de RACB at Spa, finishing behind an Aston Martin DBR1 and a Ferrari 290 MM. In 1958, Stirling Moss drove a 335 S to victory at the Cuban Grand Prix.
The career of the 335 S was cut short by a change in international regulations. In reaction to the Mille Miglia tragedy and other racing accidents, the World Championship implemented a 3-litre engine limit for the 1958 season. This rendered the 4.0-litre 335 S ineligible for championship competition, and Ferrari replaced the model with the 250 TR.
The individual history of chassis 0674 is notable for its versatility across different specifications. In its original 315 S guise, it finished sixth at the 1957 12 Hours of Sebring with Peter Collins and Maurice Trintignant, and second at the 1957 Mille Miglia with Wolfgang von Trips. After its upgrade to 335 S specifications, it set the lap record at Le Mans and achieved podium finishes in Sweden and Venezuela.
In 2016, a 1957 Ferrari 335 S Spider Scaglietti became the most expensive car ever sold at auction at that time. It was sold at the Retromobile auction in Paris for €32.1 million (US$35.1 million) following a bidding war between footballers Cristiano Ronaldo and Lionel Messi.