Construction commenced in 1966 but stopped for two years due to shortage of funds, before moving to its current location in 1971.

[15] On 23 March 2023, Tel Aviv Museum of Art was partially closed, in participation with Israel's "day of paralysis"[16] during the 2023 Israeli judicial reform protests.

[18] The Museum's collection represents some of the leading artists of the first half of the 20th century and many of the major movements of modern art in this period: Fauvism, German Expressionism, Cubism, Futurism, Russian Constructivism, the De Stijl movement and Surrealism, French art, from the Impressionists and Post-Impressionists to the School of Paris including works of Chaïm Soutine, key works by Pablo Picasso from the Blue and Neo-Classical period to his Late Period, Cubist paintings by Albert Gleizes, Jean Metzinger, several sculptures by Jacques Lipchitz, and Surrealists works of Joan Miró.

One section of the Museum displays the history of Israeli art and its origins among local artists in the pre-state Zionist community of the early twentieth century.

In 1989, the American pop artist Roy Lichtenstein created a giant two-panel mural especially for the Tel Aviv Museum of Art.

[19] The Collection includes several masterpieces, among them the painting Friedericke Maria Beer, 1916 by the Austrian artist Gustav Klimt and Untitled Improvisation V, 1914, by the Russian master Wassily Kandinsky.

In addition to a permanent collection, the museum hosts temporary exhibitions of individual artists' work and group shows curated around a common theme.