The entire cache, a total of 20,000 pieces, is expected to bring in about $100m, although there are fears the sale could dilute the Warhol brand.
In its 25th year, the Foundation, created in 1987 at the late artist's direction for the purpose of supporting contemporary visual arts, is seeking to significantly increase its endowment (from $225m to $325m) and increase its annual grant-making capacity from $13m to $18m-20m.
Christie's will conduct phased sales over a period of years using the multiple platforms now available to the auctioneer/dealer. The more valuable pieces will be offered via a series of single-artist auctions in New York (the first on November 12 comprises 350 works) but the lion's share of lots - drawings, photographs, prints, and printed graphic material - will be sold via Christie's website.
Online auctions will begin in February 2013 via a series of 'flash' auctions similar to those held for the bulk of Elizabeth Taylor's jewellery and costume collection, which will offer minor works at a range of 'approachable' price points, with some under $10,000.
Private sales from the collection will be conducted on an ongoing basis while the Foundation also plans to mark its anniversary by making additional gifts to museums.
The sale marks a shift in approach for the Warhol Foundation and follows the announcement last autumn that it had dissolved its controversial authentication board after a string of legal challenges.
It spent $7m alone fighting a lawsuit brought by Joe Simon-Whelan, owner of the 'double denied' Warhol self-portrait, who accused the board of attempting to monopolise demand for the artist's work.
The Foundation will continue to manage the copyrights to Warhol images and trademarks to his name and signature.
While few major works now remain in the collection (the Foundation has deaccessioned a handful of artworks every year since 1987), there are fears that the sheer size of this dispersal could harm a Warhol market that has proved remarkably robust and - according to statistics by ArtTactic - accounted for 17% of all Contemporary art auction sales in 2010.