Beaverton was first settled in 1822. The settlement is located on Lake Simcoe at the mouth of the Beaver River. It was called Calder's Mills, Mill Town and Milton until it was renamed Beaverton when the post office was opened in 1835. By 1869, Beaverton was a village with a population of 700 in the Township of Thorah Township in Ontario County. It was the terminus of the Port Hope, Lindsay and Beaverton Railway. The steamer Emily May plied daily between Beaverton and Bell Ewart station of the Northern Railroad. There were stages daily to Whitby and Oshawa. In 1884, Beaverton separated from the Township and was incorporated as a Village. As part of the creation of Durham Region in 1974, Beaverton was amalgamated with Thorah Township, the original Brock Township and the Villages of Cannington and Sunderland to create the newly expanded Township of Brock. Today, Beaverton is the largest community in Brock. There are three elementary schools in Beaverton and area, as well as an arena, curling club, public library, small harbour and yacht club. The local economy is based on the provision of services to the surrounding area, supplemented by some manufacturing. Tourism also plays a role; the Trent-Severn Waterway connects with Lake Simcoe a few kilometres north of Beaverton and the area attracts cottagers from other regions of the Province. Beaverton's downtown core has many stores, services, and two bars, attracting people from around the local area. Beaverton is the home of The Strand Theatre. The Old Stone Church, built in 1853 and a National Historic Site of Canada, is also located in Beaverton. The local post office services the town with lock boxes and rural routes.
The 1973, Canadian horror classic, Cannibal Girls, was filmed in the downtown of Beaverton. Sections of the downtown can all be seen. In the movie, the fictitious town that Beaverton filled in for was called Farnhamville.
The 1984 comedy, Oddballs, was also shot in the area just north along Lake Simcoe, and also at the Trent-Severn Waterway's bridge entry into the lake.