The Town Hall (more commonly known as the "Town Offices") is an energy-efficient 3-story building that was constructed in 2008, next door to its previous location at 835 Blakely Road. The 835 Blakely building is now the Town of Colchester Police Department.
Public services based in the "new" Town Hall include the Town Clerk/Treasurer, Assessor, Planning and Zoning, and Economic Development on the first floor; Public Works, Administration (Town Manager), and Parks and Recreation on the second floor. Also located on the second floor are the internal Town business departments: Finance, Human Resources, and Information Technology.
The 3rd floor attic was finished in 2017 to provide a meeting space for the Selectboard's, Development Review Board's, and Planning Commission's regular meetings. Conference rooms on the 2nd floor serve as meeting spaces for the Cemetery Advisory Commitee, Board of Listers, and Recreation Advisory Board, and for other meetings for Town-related business.