The region was under the administration of Kamnik town, whose influence reached up to Tuhinj Valley. Kamnik, first mentioned in 1061, has a long collecting tradition for first (private) collections were grounded already in 1893 by Josip Nikolaj Sadnikar (1863–1952). In 1964 the museum purchased part of this private collection, comprising antiques, religious art, paintings by Slovene artists who studied in Vienna in the late 19th century, and Chinese and Japanese art. In the same year the Municipality of Domžale joined as a founder. Until 1991 the museum was administratively merged with Kamnik Principal Library as Kamnik Cultural Centre.
The museum carries out a public service in the area from the Kamnik Alps to the Zasavje region for Kamnik, Domžale, Mengeš, Trzin, Lukovica, Komenda, and Moravče municipalities. The museum preserves, maintains and presents movable cultural heritage and collects archaeological, historical, ethnological, and art historical heritage in the region. Collections and exhibitions are prepared in cooperation with local communities, associations and individuals. It maintains extensive documentation and library, organises lectures, workshops, guided tours, and publishes different monographies and exhibition catalogues.
The internationally renowned Thonet bentwood furniture exhibition displays many objects from the former chair factory in Duplica near Kamnik, the only manufacturer of this furniture in Slovenia that operated since 1907. The chair factory endured till the end of the 1990s with Niko Kralj (1920–2013) and Branko Uršič (b. 1936) as its innovative designers.
The Life in the Kamnik Mountains exhibition presents the pastoral heritage from the nearby Velika planina and is dedicated to Vlasto Kopač (1913–2006), the architect of the ecological cottage settlement on the mountain pasture, and the ethnologist Tone Cevc (1932–2007) who in the 1990s conducted archaeological research of the area.
Apart from the exhibition on the town's history Reflections of Kamnik’s Millennia (which includes the story on the nearby excavation of the famous mammoth skeleton in 1938 that has been displayed in the Slovenian Museum of Natural History) there is also a display on the everyday life of the Kamnik bourgeoisie in the 19th century with portraits of the bourgeois family life and of the town during that period. In addition, the museum houses a castle salon, renovated in 1997, containing several Baroque and historical paintings from the end of 19th century. It is used as multipurpose room for meetings, press conferences and lectures.
In the early 1980s a lapidary collection was arranged in the arcades of the castle's side wing, including selected stones from the archaeological and art history heritage of the region, i.e., tombstone of nobleman Wiederkehr. Lapidarium was renovated in 2003.
During the 1970s an open-air museum was arranged in the castle forecourt, presenting the architectural heritage of the area which has now become nearly extinct. Four characteristic granaries from the Tuhinj Valley have been set up here, dating from the 18th and 19th centuries. The oldest one from 1793 also exhibits its entire former inventory.
The homestead is located in the old part of the small town of Trzin where Ivan Hribar (1851–1941), the mayor of Ljubljana who left a lasting impression on the city, was born. A small documentary exhibition is dedicated to him. The Municipality of Trzin completely renovated the edifice and opened it in 2013 as a local multi-purpose cultural centre.