Vernon Presley is said to have changed the finish of the Gibson Dove acoustic guitar to ebony after his son earned his black belt in karate.
It beat auction house Julien's estimate of $200,000 to $300,000 for Saturday's sale.
During a 1975 concert in Asheville, North Carolina, Presley had given the guitar to fan Mike Harris, who had kept it until now.
Another highlight of the auction was a red neoprene vinyl jacket created by Dennis Tompkins and Michael Bush for Michael Jackson to wear during the 1996-1997 HIStory world tour.
It scored more than four times the auctioneers' estimate of $40,000 to $60,000.
The highest bid reached $354,400, for John Lennon's handwritten lyrics to Beatles song ‘Being for the Benefit of Mr. Kite!’
Julien's had expected it would fetch between $300,000 and $500,000.
Overall, the sale produced lukewarm results.
Lady Gaga's first piano, estimated to be worth $100,000 to $200,000, did not find a buyer. Neither did Stevie Ray Vaughan's Fender Broadcaster electric guitar, valued at $400,000 to $600,000.
Elvis's first piano sold for $140,025, less than the $200,000-300,000 estimate.
