The former Galway City Museum, situated in Comerford House, adjacent to the Spanish Arch, was first established in 1971. and had been home to the artist Clare Sheridan. The repository began with a residual collection of medieval stones, which Sheridan had acquired from the city. The original museum closed in 2004 and was replaced by a new purpose-built museum close to Comerford House.

The new Galway City Museum was officially opened in April 2007. The building was designed by the Office of Public Works and is a Galway City Council initiative to advance the cultural and heritage life of Galway City.