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.
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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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