Founded in 1872, the Town of Babylon conducted its business through Town Board meetings held at various hotels and, on occasion, in board members' homes. The town clerk received mail and maintained records in a rented office establish in the community of his residence.
At that time, most of the town population was located within the communities of Amityville, Babylon, and Breslau (now Lindenhurst). The remainder of the town was sparsely populated and consisted mainly of farms. Town government consisted of many function, such as supervisor, councilman, town clerk, tax assessor, highway superintendent, constables, and judges. Most town officials used their homes for office space.
Opened in 1918, Old Town Hall was the first town hall erected by the Town of Babylon, and served as the seat of town government for 40 years.
In 2005, the building was placed on the National Register of Historic Places. After extensive restorations, the Old Town Hall was rededicated as the Town of Babylon History Museum on June 11, 2010, with three floors of exhibits that include the jail cells of the former Town of Babylon Police Department, the old courtroom, and a special exhibit room with an interactive multimedia table.