The community was named after John Winter, a railroad official. Winterville was incorporated in 1904. Since 1991, when the
City of Athens dissolved its city charter to form the
unified government of Athens-Clarke County, Winterville has been the only municipality located wholly within Athens-Clarke County. As of 2024, Athens-Clarke County has converted of the abandoned Athens-to—Savannah railroad spur into a paved walking trail titled "Firefly Trail". It will eventually connect to the
Georgia Hi–Lo Trail, which will become the longest paved trail and longest
arboretum in the United States. ==Geography==