The Museums Service came into existence in 1990 with the appointment of the first Museums Officer, although the then District Council had operated a museum in North Berwick since 1975.

The service now operates museums at Prestongrange, near Prestonpans; Dunbar Town House; and John Muir's Birthplace. North Berwick Museum is currently closed pending redevelopment.

In addition the service puts on exhibitions and events, and supports activities, including exhibitions, by community groups across East Lothian.