Richard Sumner and Julian Barnfield, of the Heythrop Hunt, pleaded guilty at Oxford Magistrates' Court to charges brought by the RSPCA.
Film gathered by anti-hunt monitors over four days during the 2011/12 season was played in court.
Sumner and Barnfield were the master and huntsman of the hunting group.
They pleaded guilty to four separate counts, on four separate occasions, of unlawfully hunting a wild fox with dogs.
Heythrop Hunt Ltd also pleaded guilty to four counts of the same charge.
The presiding magistrate called the RSPCA's £327,000 costs "staggering".
He said the public could question whether the charity's funds to bring the case to court could have been better spent.
Sumner was ordered to pay a £1,800 and £2,500 in court costs.
Barnsfield was ordered to pay a £1,000 fine £2,000 in costs.
In addition, Heythrop Hunt Ltd was fined £4,000 and must pay £15,000 in costs.
The prosecution said hounds had been encouraged to chase foxes -  which is banned under legislation that came into force in 2005.
Mr Cameron rode with the Heythrop Hunt on six occasions before the change in legislation.
Both Sumner and Barnfield have since retired from their positions.
An RSPCA spokesman said it was a "landmark" case.
"[It] is thought to be the first where a hunt has faced corporate charges," he said.
"It is also the first taken by the RSPCA involving the prosecution of a hunt itself."
Members of an Oxfordshire-based hunt that Prime Minister David Cameron has previously ridden with have been fined for hunting foxes illegally.