The project is the first major job to start at the £200m Waterdale scheme being developed by Muse, the urban regeneration arm of the Morgan Sindall Group.
The five-storey, 160,000 sq ft offices will house most of the council’s town centre services on one central site and become home to about 1,400 council staff.
The building features a glass-fronted council chamber that will overlook a new civic square.
The civic offices form part of the first phase of the Waterdale project, which also includes plans for a theatre.
Further phases feature a library and art showcase area, leisure developments, office developments, housing and car parking.
Dan Needham, development director at Muse Developments, said: “When complete, it will act as a catalyst for the ongoing regeneration of the wider Waterdale area by allowing the redevelopment of the vacated office buildings in future phases.”
The Waterdale regeneration project is supported financially by both Central Government and the European Union, through the Yorkshire and Humber ERDF Programme.