It has three branches in Dublin, the archaeology and natural history museums adjacent on Kildare Street and Merrion Square, and a newer Decorative Arts and History branch at the former Collins Barracks, and the Country Life museum in County Mayo.

[2] One of the earliest iterations of the RDS museum was at Hawkins Street House, where the Leskean Cabinet was displayed along with a collection of casts and busts.

With the planned expansion and development of the museum, Scouler requested that a curator or Director be employed by the RDS.

[5] The collections of both the RIA and RDS formed the basis for the Archaeology and History section of the Museum at Kildare Street.

The museum operated in the buildings at Kildare Street and Merrion Square until the late 20th century projects at Collins Barracks and County Mayo.

As of 1975, the visitable collections were summarised as "Primary: Irish antiquities and history, fine arts (excluding painting and sculpture) and natural history (excluding botany), and additionally: Egyptian, Greek and Roman antiquities, Far Eastern art and ceramics, and ethnography and zoology," with an additional collection of folk life material not on display.

This section includes famous examples of early medieval Celtic metalwork in Ireland such as the Ardagh Chalice, the Tara Brooch, and the Derrynaflan Hoard.

Many of these pieces were found in the 19th century by poor people or agricultural labourers, when population expansion led to the cultivation of land which had not been touched since the Middle Ages.

This section has displays of furniture, silver, ceramics and glassware, as well as examples of folk life and costume, and money and weapons.

Special exhibitions are mounted regularly; in summer 2007, for example, replicas of six Irish High Crosses that were subsequently shown internationally.

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