The copy of The Tales of Beedle the Bard reached £368,750 ($467,000, 439,700 euros) in the sale at Sotheby's auction house in London.
The collection of fairytales was created within the Harry Potter series and helped the young wizard and his friends defeat his nemesis Lord Voldemort.
The copy auctioned this week was given in 2007 to publisher Barry Cunningham, who gave his backing to the first Harry Potter book and thus launched a global literary craze.
"To Barry, the man who thought an overlong novel about a boy wizard in glasses might just sell... THANK YOU," Rowling wrote at the front of the book.
The collection is bejewelled with semi-precious stones and features a sterling silver mounted skull on the cover.
Rowling wrote a total of six copies of the tales by hand, which were given to those most closely connected to the Harry Potter series, while a seventh book was written for sale at a charity auction.
That copy raised £1.95 million at the Sotheby's auction in 2007, which was donated to Rowling's children's charity Lumos.
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Intense interest in the wizarding world continues nearly two decades after Rowling's first of seven volumes, Harry Potter and the Philosopher's Stone, was published in 1997.
Earlier this year a 1930s-era oak chair on which Rowling sat while writing the first two Harry Potter books sold for $394,000 through Heritage Auctions.
Rowling received the chair - one of a mismatched set of four - free when she was a young single mother living in subsidised housing in the Scottish city of Edinburgh.
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