Considered one of the most original examples in existence, it is one of only 40 built by the German marque.
Chassis 0145 had class wins at Nürburgring, Reims, Zandvoort and was fifth overall at Le Mans.
With its small size and 1.5-litre boxer engine, the 550A was nicknamed "giant killer," for its ability to chase down bigger and more powerful race cars.
Featuring a lighter space frame chassis, it is different to the ladder frame found in the 550, the same model that James Dean was killed in while driving to a race in 1955.
Weighing 70-kilograms less than the 550, and using trailing-arm suspension instead of swing axles, the little car scooted along swiftly, with the engine producing 108kW of power at 7200 rpm.
“Boasting a pedigree that distinguishes it above all others, it was a Porsche Works entrant, a veteran of four world championship races, what is believed to be the only 550A to compete in a Grand Prix," Bonhams Auctions stated.
Bonhams has not stated the estimated value of the Porsche, but in 2016 it was passed in at US $4.2-million at Pebble Beach, falling short of the $5-$6m estimation.
The auction will be taking place at Scottsdale, Arizona on January 18.