The origins of the Museum date from the 1970s when the Duke of Atholl granted the Friends of Dunkeld Cathedral permission to mount a permanent local history exhibition in the Chapter House. The Museum was refurbished in 1994. Displays cover the history of the town and the redevelopment of the reformed church. Notable local people are mentioned, as is Beatrix Potter who wrote 'The Tale of Peter Rabbit' during one of her summer holidays in Dunkeld. An archive in the rooms above the Museum contains a growing collection of photographs, records and memorabilia, including the written records of the regiment of the Scottish Horse. The Museum's single oil painting is a portrait of Charles Blair by John Zepheniah Bell. Blair was Baron Baillie of Dunkeld and the first proprietor of Menzies, a grocery business in the town.