In 1943, Solomon R. Guggenheim commissioned the American architect, Frank Lloyd Wright to design an original building to house contemporary art. Guggenheim approved the plans before his death in 1949, construction began in 1957, and the controversial building was completed in 1959, shortly after Wright's death. The unique structure was referred to by some as a "giant snail" and by others, such as architect, Philip Johnson, as "the most beautiful building in New York".

Wright himself thought the building represented the first advance in the direction of organic architecture in New York and constructed it of materials consistent with its setting adjacent to Central Park. He specified the use of as much natural light as possible inside the building and emphasized natural colors such as beige and brown.

The structure has been likened to sculpture. Cast in concrete, its spiral shape is formed by a grand cantilevered ramp that curves unbroken from the ground to the dome almost 100 feet above. The building's circular form is repeated in the shape of the galleries, the auditorium, the elevators, and in the decorative motifs on the floor and in the sidewalls in the front of the Museum. The ground floor area provides a multi-purpose space that can accomodate large scale sculpture, special events and sizeable crowds. Above the ground floor where the ramp begins, the Museum resembles a chambered nautilus with 74 niche-like bays for the display of works of art. Underneath the galleries is the auditorium, and adjacent to them is the administration building with offices for the museum staff.

Guggenheim began his art collection with works by old masters, without pursuing any particular direction. In the mid-1920s circumstances changed his course when he met and commissioned his portrait to a yong German artist, Baronness Hilda Rebay. Rebay had exhibited with avant--garde groups in Germany from 1914 to 1920 and associated with atistss such as Sonia Delaunay, Albert Gleizes, Fernand Leger, Chagall and Wassily Kandinsky. Guggenheim, who was intreoduced to her circle and vconverted by her enthusiasm for avant-garde art, began to accumulate works by these artists until the walls of his Plaza apartment were overrun. As the fame of his collection grew, he occasionally availed his home to the art world and began lending out for exhibitions. Soon Guggenheim took office space at Carnegie Hall and appointed Rebay as the custodian of the collection, which was converted in 1937 into a foundation and empowered to operate as a musuem.

James Johnson Sweeney, internationally known art critic and a former director at the Museum of Modern Art, took over the directorship upon Rebay's retirement. Sweeney proceeded to show successive selections from the colleciton as quickly as they could be prepared for the exhibition. The original collection was enlarged by the purchase of the estate of Karl Nierendorf in 1948, whcih included works by Oscar Kokoschka, Paul Klee, Chagall, Lyonel Feininger and Ernst Kirchner. Further acquisitions brought in sclpture by Constantin Brancusi, Alberto Giacometti, Alexander Archipenko, Alexander Calder, Raymond Duchamp-Villon, Aristide Maillol, Henry Moore and Max Ernst. A major purchase in 1954 was Cezanne's The Clockmaker. Arrangements were also made for the purchase of works by Braque, Miro, Picasso, and key examples by Americans Franz Kline, Jackson Pollock, Willem de Kooning, Stuart Davis and many younger artists.

The Museum is strong in a group of Impressionist and Post-Impressionist masterpieces that antedate the Museum's original holdings, and thus serves as a historical background for the collection.