The Dempster Highway is a product of the "Roads to Resources" campaign. Proposed in 1957 by the Conservative government, the campaign aimed to establish road connections with remote areas of the north to expand Canada's accessible resource pool. While the Liberal opposition called it a plan to build roads from "igloo to igloo", the program became a major platform for John Diefenbaker who consequently won a majority election in 1958.

Initially, the building of the Dempster Highway proceeded at a slow rate; maps were inaccurate and no settlement existed between Dawson City and Fort McPherson (a distance of over 500 kilometers). As a result, an army of surveyors mapped the area by land and air and a tentative route was put forth as far as Fort McPherson. By 1960, 48 kilometers of the highway were completed; 76 more kilometers were built by 1962. However, the political edge of the "Roads to Resources" was fading in light of northern economical realities and for the next seven years the Dempster Highway became the "Road to Nowhere".

In 1969 a new energy about the "Roads to Resources" project produced a relatively constant rate of construction until the highway's completion in 1979. The ten-year period took place almost exclusively during the winter months. Because of the northern latitude of the highway, construction engineers had to contend with permafrost, a layer of frozen ground that remains year round. Engineers discovered that disturbing the permafrost layer by scraping away the surface vegetation would melt the underlying ground, producing an undulating quagmire of muskeg that would render the road useless in a matter of years. In response to this factor, only trees were cut to make way for the highway. A bed of vegetation was left on the road in order that the warmth of the new highway wouldn't melt the permafrost. The winter season provided the best conditions to clear the area and deposit gravel onto the underlying vegetation. The frozen ground also prevented machinery from damaging the vegetation and spoiling any areas surrounding the highway.