Before bidding opened, the collector selling most of the 500 items reached an agreement with Caroline Kennedy and John F. Kennedy Jr to return some of their father's more "intensely personal" items.
Among the items Robert L. White agreed to hand over were two of their father's handwritten journals and a clock the president kept in the Oval Office.
As part of the agreement, the Kennedy children surrendered all claims to ownership of the other auction items, including the watch Kennedy was wearing on the day he was assassinated and the briefcase he carried with him on that trip to Dallas.
Bidding lacking enthusiasm
The bidding on Wednesday afternoon failed to excite the kind of frenzy seen during the 1996 sale of items from the estate of Jacqueline Kennedy Onassis.
A number of expected big-ticket items were removed from sale after bidders failed to meet the minimum price set by Guernsey's, the Upper East Side auction house.
A 22ft (6.7m) sloop sailed by Kennedy, the Flash II, was removed from sale after the highest bid, $800,000 (£478,000), did not meet the minimum.
Items written or signed by Kennedy attracted the most interest, including the single sheet of yellow legal paper on which he scribbled one line from his January 17, 1961 inaugural address:
"An inaugural is a beginning and an end...".
A signed Bell System telephone credit card in Kennedy's name from 1961 sold for $12,650 (£7,555), below the pre-sale estimate of $16,000 to $18,000, but well above the $1,035 (£618) paid for an unsigned 1959 membership card to the American Irish Historical Society.
"That really shows the value of a signature," said Larry Rosenbaum of EAC Gallery, an upstate New York business dealing in autographs and documents.
Still, Rosenbaum said, many of the lots were overpriced.
"I think they played on the Kennedy name," he said. "The estimates are just too high."
Mixed reactions from sellers
Kerry McCarthy, whose mother was a first cousin to Kennedy, watched with dismay.
She owns several items scheduled to be sold on Thursday, including a portrait of the Kennedy children and an ashtray.
"I'm a little surprised that the prices are so low," she said. "I'm trying to stay calm. I just hope people care for these items."
Mr White attended the sale and said the low prices would have pleased Mrs Lincoln, from whom he inherited many of the items after her death in 1995.
"I'm just glad some things are going low enough that regular people can afford them," he said. "Evelyn would have loved that."
The Kennedy children have said they feel betrayed by Mrs Lincoln.
"The number of items she took for herself, and the intensely personal character of many of them, is overwhelming," the Kennedys said in a statement.
Mr White expressed satisfaction with his settlement with the Kennedy children, but added: "The only sad part is that Evelyn's name had to be dragged down."
Kennedy Library to benefit
Tom McNaught, a spokesman for the Kennedy Library in Boston, said the returned items would be given to the library.
Earlier this week, Mr White agreed to remove 21 items after negotiating with the National Archives.
Among those were a White House writing desk and notes Kennedy made before a 1961 meeting with Nikita Khrushchev.
Two years ago, in a sale at Sotheby's to benefit the Kennedy family, bidders paid out $34.5m (£20.6m) on 5,000 items from the estate of Mrs Onassis.