The Great Northern Railway was built through what is now Whitefish in 1904, which sparked development of the town. 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. Early residents of the town worked for the railroad and nearby logging industries. By the late 1940s, with the successful construction of a ski resort on Big Mountain (a collaboration between outside developers and local businessmen) the tourism sector was becoming increasingly important. The community was named for its location near Whitefish Lake.

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 being headed to the ski resort on Big Mountain.

In December 2016, the neo-Nazi and white supremacist website The Daily Stormer published a list of six local Jews in the city along with their personal information, claiming that they were harming the business of Richard Spencer's mother and asking readers to "take action" against them. Whitefish police increased local patrols, and monitored Internet activity; Montana politicians and community groups responded with various efforts to focus attention on the question of antisemitism. On Dec. 28, 2016, Spencer indicated that he did not want to bring ongoing national attention to Whitefish with his political views, and an offer was made to call off a proposed anti-Jewish armed march in the town. The march was postponed because the proper permitting materials were not submitted and the required fee was not paid.

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Wikipedia