A 1939 Vincent-HRD 998cc Series-A Rapide led Bonhams' Spring Stafford motorbike auction on April 26, achieving £275,900 ($417,600).
It exceeded an estimate of £260,000 ($393,572) by 6.1%.
The bike has remained in the same collection since 1959 and was presented in exceptional condition.
Vincent began production of the model in 1939, but was forced to down tools following the outbreak of the second world war.
A total of 78 Series-A Rapides were made, of which only a handful have survived in working condition.
An extensively refurbished 1937 Brough Superior also sold well, realising £147,100 ($222,671).
Brough's legendary design nous and focus on quality made the model one of the best-loved British motorbikes of all time. Described as the "Rolls-Royce of Motorcycles", exceptional examples regularly achieve sums in the six-figure range.
A 1926 Coventry Eagle 980cc Flying Eight made £106,780 ($161,637).
While Coventry was among the most respected manufacturers of its era, by 1939 the Depression was taking its toll and it was forced to close.
An article in a 1925 edition of Motor Cycle magazine marvelled: "There is an undeniable fascination in owning a machine capable of seemingly illimitable speed."
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