Sotheby's Holdings told the United States Department of Justice it would plead guilty to price-fixing charges and would pay the fine.
Former Sotheby's president and chief executive, Diana Brooks, also agreed to plead guilty and co-operate with a federal investigation into the scam.
A US federal judge has delayed action on the plea to consider whether victims in a civil case would be adequately compensated.
Sotheby's current president and chief executive William Ruprecht, said the company's behaviour had been wrong and unacceptable.
Apology
"On behalf of Sotheby's I apologise to our clients for this breach of the standards of trust that they have the right to expect from us ," he said.
"I assure them that no member of Sotheby's current management played any role whatsoever in these events or was aware at any time that they were taking place."
The charges stem from a federal investigation into a conspiracy among Sotheby's and Christies to fix prices and commissions.
The firms control about 90% of the market for art and collectible auctions.
Brooks, 50, once considered one of the most powerful women in the art world, could face up to three years in a federal prison as well as fines.
'Cartel behaviour'
Federal prosecutors said the two auction houses had co-operated in setting identical commission charges for buyers and sellers as far back as 1993, continuing until last year.
The Justice Department's acting anti-trust chief, A Douglas Melamed said the deal prevented sellers getting the best price terms through negotiation.
"Those charged today were engaged in classic cartel behaviour - price fixing, pure and simple," he told the news agency Associated French Press.
"These are serious crimes, and the anti-trust division will prosecute them wherever they occur."
Hearing postponed
US District Judge Lewis Kaplan said he could not accept or reject Sotheby's plea on Thursday due to his concerns about a provision in the deal that prohibits the government from seeking restitution on behalf of victims of the scheme.
Judge Kaplan is presiding over a related civil class action in which Christies agreed to pay half of a $512m (£334m) civil settlement along with Sotheby's.
Christies has not faced criminal charges as the US Government's "leniency program," enables a company to be exempt from prosecution if it voluntarily reports a crime and satisfies other criteria.
The judge asked the parties to submit papers concerning the economic losses caused by the conspiracy and Sotheby's ability to pay the civil settlement and criminal fine.
He set a hearing or 4 December to consider the plea.