New York's original counties, ten in number, were formed during the colonial period in the year 1683. Albany county was larger than the other nine combined. It included western and northern New York and some of central and eastern New York as well as an area that became the state of Vermont.

In 1772 an enormous Tryon county that included central and western New York was cut from Albany county. Its name was changed in 1784 to Montgomery in honor of Revolutionary War hero Richard Montgomery. In 1788 a large western portion of Montgomery county became Ontario county, later subdivided into the state's western counties. In 1791 a huge central New York area was taken from Montgomery and named Herkimer. Next, in 1794 a large Onondaga county was cut from Herkimer and from Onondaga, Cayuga County was taken in 1799. From Cayuga, came Seneca in 1804. A small Tompkins county was created from southern portions of Cayuga and Seneca in 1817 and was enlarged in 1822.

What is now the town of Genoa was successively in Albany, Montgomery, Herkimer, Onondaga and finally Cayuga county. The town of Milton was formed in 1789 and covered the areas of Milton and Locke townships of the military tract which was surveyed into twenty-five 100-lot townships by July 1790, with three more added later. In 1802 Milton became smaller when Locke formed its own government. The name of Milton was changed to Genoa in 1808 and in 1817 the southernmost 60 lots of Genoa went into the formation of the town of Lansing in new Tompkins county. This left Genoa with 40 lots in an approximately 4 by 10 mile configuration stretching eastward from the east shore of Cayuga Lake.

The first settler John Clark came from Washington county in 1791. Eventually he moved to Ohio. Some other early families were Adams, Armstrong, Atwater, Bothwell, Bradley, Close, Drake, King, Lyon, Moe and Terry. The first meeting of the town of Milton was held April 1, 1794 at the home of Jonathan Woodworth located at the site of today's Lansingville in the town of Lansing. King Ferry, in the western part of the town of Genoa, was earlier called Northville and in the eastern part of the town is the village of Genoa.

Agriculturally based enterprises have been the mainstays of the town's economy. In its early history various grist mills and saw mills sprang up but exist now only in photographs or in scanty remains at their sites. Both threshing machines and steam tractors were once manufactured at Genoa village and King Ferry briefly had a glove factory. Currently, both hamlets have hotel accommodations and restaurants. In the western part of town there is a winery and a marina. In the eastern hamlet there is Smith's IGA, established in 1890, which still serves the community today. A golf course to the south in Lansing borders on the town line. Hand-crafting includes upholstering, furniture, pottery, and ceramics production. Last but not least, the famous Ithaca gun is manufactured at King Ferry.