The former Church of the Holy Spirit was built on the ruins of a yet older church in the 1770s by the Auersperg noble family and was supposedly the work of the renowned architect of that time, Johann Fuchs. In the years leading to World War II, the church ceased with its ecclesiastical purposes and between 1939 and 1966 the Museum Society for the Political Districts of Brežice and Krško had a part of its collection displayed in it.
In its first three decades, the gallery was led by the Valvasor Library, Krško which organised more than one hundred exhibitions. Later on, its custody was taken over by the local office of the Public Fund for Cultural Activities (JSKD), and in 2010 given to the Krško Culture House (which also runs the Municipal Museum of Krško and the Rajhenburg Castle).
The gallery is now sometimes compared to the Božidar Jakac Art Museum in Kostanjevica na Krki, a renowned and also church-stationed gallery for visual arts, quite similar in that most exhibitions are specially tailored for the venue.
Some of the artists who have presented their works here include the puppeteer Silvan Omerzu, the photographers Uroš Abram and Borut Peterlin, the conceptual artist Erik Mavrič, the sculptor Boštjan Drinovec, the painters Arjan Pregl and Zora Stančič, and the collective Domestic Research Society.