The town is named after Michiel Adriaenszoon de Ruyter,[3] a famous admiral in the Dutch navy.

The town is part of a region called "The Gore", a territory created by a surveying error.

Previous to 1795, DeRuyter was included in the town of Whitestown and was part of the "Lincklaen Purchase".

Jan Lincklaen once again named it in honor of a fellow countryman, Admiral Michiel DeRuyter.

The first Four-County Fair (Cortland, Madison, Chenango and Onondaga) was held in DeRuyter in 1908.

The western town line forms a border with Onondaga and Cortland counties.

New York State Route 13 passes through DeRuyter, leading north to Cazenovia and southwest to Cortland.

NY 80 crosses the northeast corner of the town, leading west to Tully and southeast to Sherburne.

The DeRuyter Central School District is located on the eastern edge of the village on Railroad Street.