In 1947, then housed in the Palais de Tokyo, its collection was dramatically increased by its first director, Jean Cassou, thanks to his special relationship with many prominent artists or their families, such as Picasso and Braque.

Since 2010, the museum has also displayed unique, temporary exhibitions in its provincial branch, the Centre Pompidou-Metz, in a 10,000-square-metre (110,000 sq ft) space divided between 3 galleries and since 2015, in Málaga, Spain, and 2018, in Brussels, Belgium.

Many styles of modern art, including Fauvism, Expressionism, Cubism, Dada, Abstract art, Surrealism are represented with works by Matisse, André Derain, Maurice de Vlaminck, Raoul Dufy, Albert Marquet, Le Douanier Rousseau, Paul Signac, Georges Braque, Pablo Picasso, Jean Metzinger, Albert Gleizes, Fernand Léger, Juan Gris, Frida Kahlo, Ernst Ludwig Kirchner, August Macke, Alexej von Jawlensky, Emil Nolde, Oskar Kokoschka, Otto Dix, George Grosz, Kurt Schwitters, Marcel Duchamp, Francis Picabia, Carlo Carrà, Umberto Boccioni, Giacomo Balla, Gino Severini, Marc Chagall, Natalia Goncharova, Mikhail Larionov, Alexander Rodchenko, František Kupka, Piet Mondrian, Theo van Doesburg, Paul Klee, Wassily Kandinsky, Kasimir Malevich, Jacques Villon, Robert Delaunay, Sonia Delaunay, Georges Rouault, Balthus, Max Beckmann, Constantin Brâncuși, Alexander Calder, Chaïm Soutine, Amedeo Modigliani, Kees van Dongen, Jean Arp, Giorgio de Chirico, André Breton, Magritte, Max Ernst, Joan Miró, Man Ray, Alberto Giacometti, Salvador Dali, Nicolas de Staël, André Masson, Yves Tanguy, Jean Tinguely, Simon Hantaï, Yves Klein, Jackson Pollock, Mark Rothko, Barnett Newman, Willem de Kooning, and Francis Bacon.

[3] In 2011, Centre Pompidou admitted that it held three paintings, Les Peupliers (Poplars), Arbres (Trees), and Composition by the artist Fédor Löwenstein that had been looted during the Nazi occupation of France.

[4] In 2021, after the French government restituted a looted Max Pechtstein painting to the heirs of Hugo Simon, the Centre Pompidou held an exhibition in a tribute to the persecuted art collector.