Solomon R. Guggenheim, born into a wealthy mining family, had been collecting artwork since the 1890s and had held exhibitions in his private apartment at the Plaza Hotel before opening the "Museum of Non-Objective Painting" in 1939 in a former car showroom at 24 East 54th Street. The "non-objective" part of the museum's title refers to what we typically call abstract art today, where artists express themselves using visual language without attempting to represent physical objects. Guggenheim's museum would move to its current location along Central Park in 1959, into a building that Robert Moses described as an "inverted oatmeal dish".

Although constructed on a limited budget and met with criticism of its architecture, the Frank Lloyd Wright-designed building would take its place along Fifth Avenue and become a symbol of New York City's art scene. The museum is one of the city's most-visited attractions, with just over 1 million visitors annually.

After 16 years of planning and construction, the building opened after both Guggenheim's and Wright's deaths, in 1949 and 1959, respectively. It was only after Solomon Guggenheim's death that the Museum of Non-Objective Painting was renamed in 1952 in honor of its founder and the collection of art he had spent his life acquiring.

The museum's curved exterior of formed cement has become iconic, but Frank Lloyd Wright originally proposed that the building would be colored red, instead of bright white!

While the building was meticulously planned by Frank Lloyd Wright to utilize light from above, the original skylight at the top of the spiral building had been covered over and had to be replaced in 1991 with new thermal glass that filters out harmful UV and infrared light that could be damaging to the artwork. The museum's extensive three-year, $24 million renovation in the 1990s also involved constructing a tower near the museum to add gallery space, office space, and storage capacity, similar to a ten-story tower that Frank Lloyd Wright had initially planned for the site, but had been scrapped from the final plan due for financial reasons.