The name of the town came from a nearby mountain range called the Moccasin Mountain range. The name of the mountains come from the look with densely forested lodge pole pine trees; the Native Americans thought they looked like moccasins, thus giving the mountains and the town a name.
Moccasin has also been hit hard by devastating wildfires that struck the area in 1916, 1919, 1922, and 1955. The town never really recovered from the fires which burned an entire block of buildings.
Moccasin began as a homestead community. In 1908 the Montana State legislature created the MSU Central Agricultural Research Center, 3 miles west of Moccasin. The purpose of the centre was to teach dry land farming techniques to the newly arrived homesteaders. Even after the homesteaders bust, the centre went on to develop machinery and new crops, improving the area's wheat yields.
The nearby Ackley Lake State Park, named after an early settler and frontiersman, offered diverse water sports opportunities. Stocked with rainbow trout, the lake is often good angling for 10 to 15 inch fish. The elevation of the park was 4,336 feet and is 160 acres in size.