For around two thousand years, the Southern Tutchone people had seasonal hunting and fishing camps in the area of present-day Haines Junction. The original name of the area was "Dakwakada", a Southern Tutchone word meaning "high cache". It was common for Tutchone people to use raised log caches to store food year-round or temporarily while they hunted and fished in an area.
The Haines Junction area was also important for trade between the coastal and interior peoples. It lies at the interior end of the Chilkat Pass, one of only three passes that allowed travel between the coast and the interior, which was used extensively for trade between the coastal Tlingit and Southern Tutchone people.
The current town of Haines Junction was established in 1942 and 1943 during the construction of the Alaska Highway. In 1943, a second highway, the Haines Highway, was built to connect the Alaska Highway with the coastal town of Haines, Alaska, over the Chilkat Pass. Situated at the junction of these two highways, Haines Junction was a construction camp and a supply and service centre for the U.S. Army Corps of Engineers building the highway. The 626-mile (1,007 km) Haines–Fairbanks petroleum pipeline was constructed in 1953–55, and a pumping station was built just north of Haines Junction.
By road, Haines Junction is served by the Alaska Highway and the Haines Highway (Yukon Highway 3). By air, it is served by the Haines Junction Airport.
The widely publicised local tourist information centre, funded by Parks Canada, is only open regularly during the peak May 25–September 25 season. Local residents and some out-of-town commentators suggest that year-round operation would boost local income levels and job opportunities, as well as increase winter tourism to the region.