After three years of planning, the museum has been established in a former Fire Service command unit.
This is a specialised fire truck, built in 1970, and once used in the on-site management of major fire incidents in Dunedin.
Gary Byford, a restoration society committee member, said he had been working intensively on the project in recent months.
"I'm very pleased the way it's turned out."
"It's going to be great for the general public to see things they don't normally see."
Organisers said the museum would raise community awareness of the history of the Dunedin Fire Brigade, which was New Zealand's first city-based brigade.
The travelling displays will also help raise awareness about the brigade's 150th anniversary, which will be celebrated next year.
Restored fire engines from the society's collection take part in many community events, including Warbirds Over Wanaka and Dunedin's Santa Parade.
In future the mobile museum will also be available for such occasions, organisers say.
Several New Zealand firefighting "firsts" achieved by Dunedin firefighters over the years are highlighted in the displays.
In 1874, the Dunedin brigade became the first in New Zealand and Australia to use a specialised leather smoke helmet, enabling firemen to enter burning buildings.
Air was pumped into the helmet via a hose from outside the building.
In 1946, Dunedin also became the first brigade in the country to establish radio communications between the Central Fire Station and two fire vehicles.
Museum visitors will also be able to see an array of other fire helmets used over the years, as well as a chemical hazard suit and a wide range of other equipment, including fire extinguishers and breathing apparatus.
• The restoration society has a special relationship with the Otago Settlers Museum and undertakes many activities to support the museum's programmes.