The town was named after John Conklin, a railway employee. Originally, the settlement sat at the extreme northwestern end of Christina Lake, near the outlet of the Jackfish River. However, when the Alberta and Great Waterways Railway (later part of the Northern Alberta Railways) reached the area in 1921, the town was physically relocated to sit directly alongside the new railway tracks, which helped integrate it into broader provincial trade routes. The Post Office opened May 15, 1924.

For a few decades mid-century(1940-1960), Conklin evolved into a bustling regional hub driven by local wildlife and natural resources. Conklin served as a vital collection point for trapping. Local mink farms and trappers brought pelts via canoe and dogsled to the Conklin railway siding to be shipped out to southern markets. Christina Lake supported a heavy commercial fishing industry. A dedicated fish processing plant operated right at the outlet to the Jackfish River during this period.