A 1927 Brough Superior 981cc SS100 Alpine Grand Sport project led Bonhams' October 18 Stafford Sale, achieving £259,100 ($401,229).
The model was designed by George Brough, who spared no expense on its creation.
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It remains the definitive motorbike of its era, with projects made up of original parts proving a huge draw for collectors.
This specimen has been in the collection of the same owner since 1970 and comes with its original logbook.
Ben Walker, Bonhams head of motorcycles, comments: "With great looks, excellent engineering and a prestigious reputation, it's no surprise Brough Superior continues to prove popular, with enthusiasts willing to spend strong figures for both complete bikes and restoration projects, as we've witnessed at today's sale, where the 1927 Brough Superior 981cc SS100 Alpine Grand Sport project was the highest grossing lot."
Other top selling lots at the prestigious motorbike auction included a 1930 Indian Model 402 four motorcycle combination, which set a new record for the model at £97,700 ($151,293).
Described by Bonhams as "the Duesenberg of motorcycling", the Indian Four is known for its elaborately decorative fenders.
Its good looks have ensured it remains one of the most popular models Indian released.
"It's been an excellent weekend at Stafford, with a two-day sale that has grossed an incredible £3.6 million, a new record for the sale," said Walker.
It is Europe's highest ever grossing motorbike sale.
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