It and most of the city were destroyed by Allied bombing during the Second World War and the building and its collections both had to be recreated in the post-war period,making it what one author[who?]

On 20 September 1938 the director general of fine arts at the ministry of national education in Paris invited curator Jean Lachaud to produce a list of artworks to be protected in case of war.

The artworks were unframed, rolled and crated but a lack of manpower and transport prevented their being moved and some of them were damaged in a three hour bombing raid on 31 March 1941 against three German heavy cruisers then in harbour at Brest.

The rubble was pillaged, leading to the "Dépêche de Brest" on 12 July demanding that the city's inhabitants return objects stolen from the museum's ruins.

Also represented are the Pont-Aven School and Les Nabis (Henri-Gabriel Ibels, Henri Delavallée, Claude-Émile Schuffenecker, Henry Moret, Armand Seguin, Émile Bernard, Maxime Maufra, Édouard Manet, Pierre Bonnard, Georges Lacombe, Paul Sérusier, Maurice Denis, Julie Delance-Feurgard, Albert Clouard and Jean-Julien Lemordant), Orientalists such as Paul Leroy, Charles de Tournemine and Anna Quinquaud and Symbolists such as Edgar Maxence, Henri Martin, Alexandre Séon, Eugène Carrière, Lucien Levy-Dhurmer, René Ménard, Charles-Marie Dulac and Léon Spilliaert.