Its brief covers the territory of the old Otago Province, that is, New Zealand from the Waitaki River south, though its main focus is the city of Dunedin.

Its collections evolved reflecting these changes but remain focused on the historical period, i.e. since James Cook's first visit to southern New Zealand in 1770.

Comparable museums in two other New Zealand cities, Auckland and Wellington, were closed after the second world war and their collections dispersed.

The buildings were extensive, the collections considerable and varied, comprehending furniture, apparel, technology - including household appliances and vehicles - as well as archives and works of art.

The Dunedin City Council provided grants increasingly covering costs and in 1991 took over the museum's ownership and operation.

The neighbouring former bus station of New Zealand Railways Road Services, designed in 1939 by James Hodge White (1896-1970), was acquired.

This structure, one of Dunedin's more notable examples of art deco architecture, is now used to house vintage transport and related machinery.

In 2006 the city council decided to proceed with extensive additions to the north and east of the Burnside complex to consolidate the collections on a single site and to provide better conditions for their storage and exhibition.

The two Burnside wings detail the history of the region from pre-European times, through the Otago gold rush to the end of the nineteenth century, and include costumes, dioramas, and multimedia displays.

The former entrance link between this area and the former bus depot has been turned into a research centre and military history display with a Roll of Honour remembering all those from Dunedin who have died at war.

A traditional Chinese garden has been constructed on land immediately behind the museum's southern wing, and opened to the public on 8 July 2008.