The town, part of the Sadaquada Patent, was first settled in 1784, the first time any permanent settlement was made in the county. The Town of Whitestown was formed in 1788, before the creation of Oneida County, with a size of 12 million acres (49,000 km²).
It is known as the "Mother of Towns" because of the many towns and counties formed from its expanse. The Town of Paris and the Town of Steuben were formed from Whitestown in 1792. The Town of Cazenovia was formed in 1793. The Town of Augusta was formed in 1798. Utica was formed in 1817. The Town of New Hartford was formed from Whitestown in 1827.