Long before the first Europeans came to Whitefish, native American tribes inhabited the area, most notably the Kootenai, the Pend d’Oreille, and the Bitterroot Salish. The Kootenai lived in the area for more than 14,000 years, inhabiting the mountainous terrain west of the Continental Divide, and traveled east of the divide for occasional buffalo hunts.

Though trappers, traders, and waves of westward immigrants passed through the area during the second half of the century, it wasn’t until 1883 that the first permanent settler, John Morton built a cabin on the shore of Whitefish Lake, just west of the mouth of the Whitefish River. Morton was joined by the local logging industry forefathers—including the Baker and Hutchinson brothers—in the early 1890s.

Logging crews “boomed-up” their logs behind a dam built at the river mouth by the Boston & Montana Commercial Company, which, when opened, created a rush of water that helped float the logs down the river to Kalispell. The Great Northern Railway was built through what is now Whitefish in 1904, which sparked the development of the town.

The town incorporated in 1905. The area was originally known as Stumptown due to the abundant amount of timber that had to be cleared to build the town and railroad and because tree stumps were left in the streets throughout downtown. Early residents of the town worked for the railroad and nearby logging industries.

In 2006, over 68,000 passengers embarked and disembarked through the historic Whitefish Depot, a stop on Amtrak's Empire Builder line, with some percentage of those headed to the ski resort on Big Mountain. Skiing has been part of the Whitefish area for more than 50 years. In 1937, the Whitefish Lake Ski Club obtained a special permit from the U.S.

Forest Service enabling them to build cabins and trails in the Hell Roaring Creek region. Great Falls businessmen Ed Schenck and George Prentice recognized the area’s potential and, after World War II, began efforts to develop a full-fledged ski resort on the mountain with local people donating labor, preparing the slopes, even giving up free time to help push through an all-weather mountain road.

On December 14, 1947, Schenck, Prentice, and a thousand townsfolk stood on the newly christened ski resort's slopes to watch the brand new T-Bar lift bring their community vision to life.The town started a curfew siren in 1919 that they called the "ding-dong ordinance". The historic siren was restored to the new city hall.