Just when it seemed the high-flying art market couldn’t soar any higher, paintings and sculptures from the collection of the Microsoft co-founder Paul G. Allen, hit the $1 billion mark at Christie’s New York on Wednesday night, making it the biggest sale in auction history.

The first of two Allen sales, it shattered a six-month-old record of $922 million set at Sotheby’s for art from Harry and Linda Macklowe, squabbling spouses whose divorce settlement included the sale of their collection.

Where a price of $100 million used to signify entry to a rarefied club of auction record holders, the salesroom scarcely applauded as several lots exceeded that mark, including Georges Seurat’s “Les Poseuses, Ensemble (Petite version)” ($149 million, with fees); Paul Cézanne’s 1888-90 Cubism precursor “La Montagne Sainte-Victoire” ($138 million); van Gogh’s verdant scene of Arles, “Verger avec cyprès” ($117 million); and Gustav Klimt’s 1903 autumnal “Birch Forest” ($105 million).

The Klimt sale broke the previous high for the artist at auction: $88 million for “Portrait of Adele Bloch-Bauer II” in 2006, the same year Allen bought his Klimt for about $40 million.

Attesting to the apparent immunity to world events of the uppermost sliver of the art market, bidding at the sale was vigorous on several lots (there were four on the Seurat). Some art experts said the lack of a potentially market-rattling political rout in Tuesday’s election gave buyers greater comfort in parting with their funds for pretty pictures.

“People want to put their money into hard assets,” said the dealer Nicholas Maclean of London and New York.

The auction of the art of Allen, who died in 2018, generated a level of excitement not typically seen in an often-jaded art world. Among the usual suspects in the room — such as the dealers Larry Gagosian, David Zwirner, Amalia Dayan and Joe Nahmad — those who had flocked to the auction included the Christie’s owner, François-Henri Pinault, who sat in one of the more discreet skyboxes.

“We are seeing a very focused activity from collectors in response to rare masterpieces coming to market,” the dealer Dominique Lévy said. “A sale like this does not reflect the art market at large, but the appetite for exceptional rare works. It’s very important to understand the patina of this unique legendary provenance.”

The sale hit the $1 billion mark at Lot 32, Alberto Giacometti’s graceful standing nude “Femme de Venise III,” which sold for $25 million on an estimate of $15 million to $20 million. This development, however, was not announced by the auctioneer; those in the room were unaware that the art market had just made history.

Many of the night’s buyers were bidding by phone in Asia. “Buyers in Asia are very much alive,” Gagosian said. “When something is rare and great, they are strong.”

Right from the start, the first three lots sold well above their estimates. These included Edward Steichen’s dark, haunting 1904 “Flatiron,” showing the Flatiron Building in New York. At $12 million — four times the high estimate — it set an auction high for the artist. It was the second highest price ever paid for a photograph, after Man Ray’s 1924 “Le Violon d’Ingres,” which went for $12.4 million at Christie’s last May.

More than 20,000 people viewed the collection in advance, with lines as long as two hours stretching down Rockefeller Plaza in midtown. Such previews often attract art fans who are eager to see masterworks before many of them disappear into private collections.

The sale had been eagerly anticipated by collectors, not only for its record-setting estimates but because of the range of blue-chip works represented in Allen’s collection, which he started in the 1980s.

The artworks — more than 150 of which came to Christie’s, which will offer 95 of them in a day sale on Thursday — spanned 500 years of history. It ranged from Botticelli’s classical “Madonna of the Magnificat” (mid-15th to early 16th century), which sold for $48 million on an estimate of $40 million, to Wayne Thiebaud’s whimsical array of desserts, “Café Cart” (2012), which sold for $6 million on an estimate of $3 million to $5 million.

It included a fiery abstract painting by Jasper Johns, “Small False Start,” an early work from 1960, which sold for $55 million (the estimate was $45 million to $65 million). The work of blues, red, yellow and orange broke the artist’s $36 million record, set in 2014, for a flag painting bought by Alice Walton. “It tells the story of his relationship to collage,” said the art adviser Allan Schwartzman, who has a professional relationship with the Allen estate. “It’s an exquisite object.”

The collection was heavy on figurative works like Édouard Manet’s painterly snapshot of a paddling gondolier, “Le Grand Canal à Venise,” and David Hockney’s “The Conversation,” which depicts the curator Henry Geldzahler and the writer Raymond Foye engaged in a tense conversation.

David Nash, who served as an art adviser to Allen, said the tech magnate had brought the same enthusiasm to buying paintings as he had to all of his other interests, which included sports teams, marine biology and brain research. “The Seurat is probably an irreplaceable painting — and the van Gogh and the Cézanne,” he said.

At the same time, some art experts said the sale was a better barometer of Allen’s buying prowess than of his singular aesthetic passion. “It’s like the tech mind — everything is in amazing condition, vivid colors, not too disturbing, not too sexual — like a numbers or computer guy would think it through; every one of them is a near perfect example,” said the dealer and collector Adam Lindemann. “I don’t think the collection says much about him. You can walk through the whole thing and not come away with a feeling about Paul Allen. It’s very analytical and very precise.”

Schwartzman, the art adviser, on the other hand, said he saw in the collection “someone who had a very personal connection to the works he bought.”

He added, “I find it moving that someone who has had so much impact on how the world functions today also had this strong and personal response to the artist and the hand.”

Allen was somewhat ahead of his time in collecting works by women, including Agnes Martin, Louise Bourgeois and Barbara Hepworth. And on Wednesday, Georgia O’Keeffe’s “White Rose with Larkspur No. 1” sold for $27 million, more than four times the low estimate of $6 million.

Christie’s guaranteed the entire sale, meaning the auction house had agreed to pay the Allen estate a minimum negotiated price for the whole cache. Christie’s then in turn offset that risk by securing minimum bids on many of the lots from third parties — people who agreed to a purchase price in advance, thereby ensuring they could buy the work if it didn’t exceed the guarantee.

All of the proceeds went to philanthropy, as Allen directed; his estate has not disclosed the beneficiaries, perhaps to avoid alienating potential buyers who did not agree with the charitable causes.

The high prices affirmed Allen’s discerning taste, as well as his eye for art that was likely to appreciate. In 2016 he sold Gerhard Richter’s painting of an American fighter jet for $25.6 million, more than double the $11.2 million he had paid a decade before, and in 2014, he sold a Mark Rothko painting for $56.1 million, for which he had paid $34.2 million in 2007.

“He was a top-of-the-market buyer,” said Amy Cappellazzo, a prominent adviser and former auction executive, “without a lot of competition.”

Robin Pogrebin

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