The region was settled in the late 1600s under the Schuyler Patent. The land was stolen from local natives who could not read the Dutch written deed. Prior to 1812, Red Hook was part of the Town of Rhinebeck. Because Rhinebeck, as well other towns, had populations over 5,000 residents, the Albany Legislature authorized the separation of these two precincts on June 12th to accommodate and encourage public attendance at town meetings via horseback or carriage. The first documented Town of Red Hook meeting was on April 6, 1813 in a local inn and held yearly afterwards as required by law. Wealthy landowning farmers oversaw the maintenance of their assigned roads with the help of their farm workers and neighbors. The Red Hook Society for the Apprehension and Detention of Horse Thieves is thought to be one of the oldest formal organizations in the state and still holds an annual meeting.

• Annandale-on-Hudson -- A hamlet in the northwest part of the town by the Hudson River. Because this community does not have a well-developed business district, students of Bard College often use the Villages of Tivoli and downtown Red Hook as "college towns."
• Barrytown -- A hamlet south of Annandale-on-Hudson. The north junction of NY 9G and NY 199 is known as Barrytown Corners.
• Cokertown -- A hamlet in the northeast part of the town, located on County Route 56.
• College Park -- A housing development east of Bard College.
• Fraleighs -- A hamlet in the eastern part of the town.
• Kerleys Corners -- A hamlet near the north town line at the junction of US 9 and County Route 78.
• Linden Acres -- A housing development northwest of Red Hook village.
• Red Hook -- The Village of Red Hook.
• Red Hook Mills -- A hamlet north of Red Hook village.
• Tivoli -- The Village of Tivoli is in the northwest part of the town by the Hudson River. The West side of NY 9G is Tivoli, while the east is still considered the town of Red Hook.
• Spring Lakes -- a small hamlet along County Route 55.
• Upper Red Hook -- A hamlet north of Red Hook village.