The maroon beauty achieved $396,000 at what is the second running of the event, which organisers hope will become a yearly tradition.
The vehicle, which Auctions America describes "as an undisputed masterpiece of classic era design", narrowly missed its $400,000 low-end estimate, perhaps due in part to bad wear to the body number, which has left its exact digits in some doubt.
However, the fact that the classic car had remained in such good driving condition ensured that it was not short of suitors.
The Auburn Speedster was priced at $2,245 when it was unveiled in 1935, in the knowledge that the company would make a $300 loss on every sale. Bosses hoped that it would stimulate interest in the company.
A 1934 Auburn Twelve Salon Phaeton was not far behind at the auction, achieving $292,600 at the long weekend of events that realised $18.5m in all, with 60.5% of lots selling.
Other highlights for classic car collectors included a 1953 Cadillac Eldorado, which made $280,500, and a 1958 Cadillac Eldorado Biarritz, which came in at $179,300.
On the motorcycle front, a 1930 Excelsior Super-X Streamliner went for $33,600, while a 1917 Indian Twin achieved $31,472.
"We are very happy with the results from our debut motorcycle offering in Auburn," commented Glenn Bator, the head of Auctions America's vintage motorcycle division.
"The offering was very well-received and Motorcycle Alley, as it was described onsite, was a hive of activity throughout the weekend."
Paul Fraser Collectibles will bring you further classic car and motorcycle news throughout the course of the year.
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