Built in 1904, the museum has three permanent exhibitions: "Ancient Origins" details the borough's past from prehistory to Anglo-Saxon times; "Town of Kings" charts Kingston's development as a market town from the medieval period until the 1940s; and "Eadweard Muybridge" presents material related to the noted photographer, a native of Kingston.

This scheme to record the changing landscape of the borough was the brainchild of Reginald Brill, head of the former Kingston School of Art, and ran from 1955 to 1971.

The Friends of Kingston Museum relaunched the scheme in 1997, and additions to the collection are made annually and displayed as part of a rolling programme in the art gallery stairwell.

Other highlights on display are stained-glass windows from the old Town Hall in the Market Place, a Roman altar with inscription, an Anglo-Saxon skeleton and a model of Nipper, the dog featured in the "His Master's Voice" logo, who was buried under what is now Kingston's Lloyds Bank in 1895.

Muybridge spent his career in America, and there are a number of collections in the US which also hold significant material relating to his work.