The museum is more constellation than building. In Vilnius alone there are five distinct sites: the Vilnius Picture Gallery for old masters, the National Gallery of Art for modern and contemporary work, the Radvila Palace Museum of Art in a restored Baroque palace, the Vytautas Kasiulis Museum of Art devoted to a single twentieth-century émigré painter, and the Museum of Applied Arts and Design. A small Clock and Watch Museum holds horology. Out on the Baltic coast there are three more: the Pranas Domšaitis Gallery in Klaipėda, the famous Palanga Amber Museum tucked inside a nineteenth-century counts' palace, and the Pamarys Gallery. About 350,000 visitors a year move between these venues, often without realizing they are inside one institution.

The museum's history is a kind of compressed twentieth-century Lithuanian story. The first concrete plans came in 1933, under the Polish administration that controlled Vilnius between the wars; that body decided to establish a Vilnius City Museum and began assembling collections. The first exhibitions were not held until April 1941, by which point Lithuania had been annexed by the Soviet Union, and the museum opened under the name Vilnius State Art Museum. From 1966 onward it was called the Lithuanian Art Museum. Only in January 1997, six years after independence, did the new Lithuanian government grant it national status. Each name change in that sequence corresponds to a different country claiming the same building and the same paintings, which is a fairly Lithuanian thing for a museum to have lived through.

The collection runs to roughly 250,000 objects. About 2,500 paintings span the sixteenth through nineteenth centuries, and many of these are portraits of nobles and clergy of the Grand Duchy of Lithuania, the rambling multi-ethnic state that once stretched from the Baltic to the Black Sea. There are religious works pulled from Lithuanian churches and cloisters before they could be lost. The drawings cabinet holds more than eight thousand sheets by Italian, German, French, Flemish, Dutch, Polish, English, and Japanese hands from the fifteenth to twentieth centuries, an unexpectedly cosmopolitan archive for a country its size. Twentieth-century holdings are vast: more than 12,000 works from the first half of the century and over 21,000 from the second. The applied arts wing has amber, ceramics, porcelain, glass, textiles, leather, furniture, coins. There is a deep folk-art collection of carved wooden chapels and roadside crosses, the kind of vernacular religious art for which Lithuania was famous before mass production replaced the village carver.

Two quieter institutions sit inside the museum's larger structure. The Pranas Gudynas Centre for Restoration, named for the long-serving postwar director who built it, is the conservation lab that every museum in Lithuania now uses. Its restorers handle paintings, archaeological objects, and historical artifacts that come in from across the country. The Lithuanian Museums' Centre for Information, Digitisation and LIMIS handles the slow, patient work of getting Lithuania's collections online and into shared European catalogs through the LIMIS system. Visitors do not see either operation. They make the rest of what visitors see possible. The current director, Arūnas Gelūnas, has run the museum since 2019, the latest in a line that includes Adolfas Valeška, Pranas Gudynas, and Romualdas Budrys, names that map onto the museum's wartime, Soviet, and post-independence lives.