In a sale that generated interest from around the world, the race car fetched 28 million euros plus premiums and taxes taking the overall price to just over 32 million euros.
The Spider -- which beat the record set in 2014 when a 1962 Ferrari 250 GTO sold for what was the equivalent of 28.9 million euros -- finished sixth in the Sebring 12 Hours race in 1957 and second in the Mille Miglia 1,000-mile (1,600-kilometre) road race in Italy.
Thereafter the car was returned to the factory to have its engine size boosted from 3.6 to 4.1-litres -- boosting power from 360 to 400 horsepower, allowing a top speed of 300 kilometres an hour (186 mph).
The Ferrari enabled the Italian manufacturer to win the Constructors' World Championship title in 1957.
The identity of the purchaser of the Spider was not revealed following Friday's deal but is US-based, according to Matthieu Lamoure, director general of Artcurial motorcars.
"Clearly, we won't soon forget," Lamoure told journalists after the hammer came down on the record sale, bidding having started at 20 million euros.
The sleek machine had belonged to the family collection of late French racing driver Pierre Bardinon, who died in 2012.
Legendary British driver Mike Hawthorn drove the Spider in the Le Mans 24-hour race in 1957.