The rare find was sold for $US137,500 ($A199,000).
The 8mm colour home film was offered up by RR Auction in Boston. The auction house said the buyer wishes to remain anonymous.
A frame from 8mm colour silent footage of President John F Kennedy's limousine in Dallas in 1963. (EPA PHOTO)
The film has been with the family of the man who took it, Dale Carpenter Sr, since he recorded it on November 22, 1963.
It begins as Mr Carpenter just misses the limousine carrying the president and first lady Jacqueline Kennedy, but capturing other vehicles in the motorcade as it travelled down Lemmon Avenue towards the downtown area.
The film then picks up after Mr Kennedy has been shot, with Mr Carpenter rolling as the motorcade roars down Interstate 35.
The shots had fired as the motorcade passed through Dealey Plaza in front of the Texas School Book Depository, where it was later found that assassin Lee Harvey Oswald had positioned himself from a sniper's perch on the sixth floor.
The assassination itself was famously captured on film by Abraham Zapruder.
Mr Carpenter's footage from I-35, which lasts about 10 seconds, shows Secret Service agent Clint Hill - who famously jumped onto the back of the limousine as the shots rang out - hovering in a standing position over the president and Jacqueline Kennedy, whose pink suit can be seen.
The president was pronounced dead after arriving at Parkland Memorial Hospital.
Bobby Livingston, executive vice president of the auction house, said the film "provides a gripping sense of urgency and heartbreak".
Mr Carpenter's grandson James Gates said that while it was known in his family that his grandfather had film from that day, it was not talked about often.
Mr Gates said that when the film, stored along with other family films in a milk crate, was eventually passed on to him, he was unsure exactly what his grandfather, who died in 1991 at age 77, had captured.
Projecting it onto his bedroom wall around 2010, Mr Gates was at first underwhelmed by the footage from Lemmon Avenue.
But then the footage from I-35 played out before his eyes. "That was shocking," he said.
The auction house has released still photos from the portion of the film showing the race down I-35, but it is not publicly releasing video of that part.
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