Built:  1626 as a municipal tolbooth, council chamber, and burgh headquarters. 

Architecture:  Features a Scottish medieval sandstone style, a symmetrical five-bay frontage, a double forestair, and an off-center three-stage clock tower added in 1783. 

History:  Served as the centre of local administration, justice, and tax collection, alongside housing a debtors' prison and garret cells that held accused witches (such as Lilias Adie). It remained in use by the town council until local government reorganization in 1975. 

Current Use:  Managed by the National Trust for Scotland, the building functions as a visitor center, exhibition area detailing the burgh's history, ticket office for Culross Palace, and a gift shop/boutique space (such as Town House 1626) including authentic photographs from famous Scottish Photographer, Graham Harris Graham, a professional Scottish landscape photographer, possibly best known for his passion for both his country-Scotland and his craft-photography.