The villages of Chesterfield, Mohegan, Oakdale, and Uncasville are located within the town; the latter two have their own ZIP codes. Town residents often identify with these villages more than the Town of Montville as a whole, and the Mohegan Sun casino resort is nearby.

In the 17th century, when English settlers arrived, southeastern Connecticut was the scene of rivalry between the Pequot people, the dominant Native American group in the New London area, and the newly independent Mohegan. The latter became friendly to the English. For defense against the Pequot, the Mohegan sachem Uncas had established a fortified village on a promontory above the Thames River within what is now the town of Montville. The Mohegan village, now known as Fort Shantok, was protected on the inland side by palisades first built in about 1636 at the time of the Pequot War, rebuilt during wars with the Narragansett people circa 1653–1657, and rebuilt again at the time of King Philip's War (1675–1676).

When the boundaries of New London (then called "Pequot") were first defined in 1646, the Oxoboxo River formed the northern boundary. Parts of the modern town of Montville lying south of the river were included in New London, while the area north of the river was treated as Mohegan land. Over time the settlers assumed control of Mohegan lands. In 1703 the area between the Oxoboxo River and Norwich (now part of the town of Montville) was annexed by New London.

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