The museum was established in 1914 by the members of a local society of fans of the fine arts, as a monument to artist, Vasily Vereschagin.

It included works which were donated by the Academy of Arts, Alexander's III Russian museum, and items which were sent by V. V. Vereschagin's widow, Lydia Vasilyevna.

On the eve of the Great Patriotic War, the collection museum totaled almost 1000 works.

Today Vasily Vereshchagin's Museum of Art has the most comprehensive collection of works by contemporary artist of Nikolaev: M. Ryasnyansky, V.I.

There is a separate hall in the museum where works of West European art are shown.

According to the decision of the presidium of the Ukrainian Academy of Arts, the museum was awarded a silver medal on July 28, 2009, for the promotion of art, for merits in aesthetic education of young generation, and in view of the 95th anniversary of the foundation day.