The November sale of more than 150 pieces spanning 500 years will be "the largest and most exceptional art auction in history", Christie's said on Thursday.
The works include La Montagne Sainte-Victoire by French painter Paul Cezanne, valued at more than $100 million, the auction house said.
Christie's, with the backing of Allen's estate executors, said all proceeds will go to charitable causes, as per the wishes of Allen, who was an avid art collector, innovator and philanthropist.
Allen, who died in 2018 aged 65, co-founded Microsoft with Bill Gates in 1975. Together, they came up with the PC operating system that made a fortune for the US technology company.
Allen left in 1983 owing to health problems and a deteriorating relationship with Gates, who remained in charge of Microsoft until 2000.
The auction record for a private collection was set this spring by US couple Harry and Linda Macklowe, with $922m fetched in sales conducted by Sotheby's.
Other than the work by Cezanne, the Allen collection features a work titled Small False Start by American painter Jasper Johns, valued at more than $50m, The New York Times reported.
Christie's did not detail what else is in the collection, but a travelling exhibition in 2016 gave a glimpse of the richness of the Allen art trove.
It features works by Monet, Manet, Klimt and others.
This year is shaping up as one of the biggest in the art world.
Besides the Macklowe auction, an Andy Warhol portrait of Marilyn Monroe sold in May for $195m — a record for a piece of 20th century art.
Christie's chief executive Guillaume Cerutti said the Allen auction will be like no other.
"The inspirational figure of Paul Allen, the extraordinary quality and diversity of works, and the dedication of all proceeds to philanthropy, create a unique combination that will make the sale of the Paul G Allen Collection an event of unprecedented magnitude," Cerutti said.
"To Paul, art was both analytical and emotional. He believed that art expressed a unique view of reality — combining the artist's inner state and inner eye — in a way that can inspire us all," said Jody Allen, the executor of the estate.
"His collection reflects the diversity of his interests, with their own mystique and beauty."