The commissioner is appointed by the federal government and, in contrast to the governor general of Canada or the lieutenant governors of the Canadian provinces, is not a viceroy and therefore not a direct representative of the Canadian monarch in the territory eo ipso.

By the 1960s, the Commissioner had formed an executive committee that included some members of the elected Territorial Council, in essence a cabinet.

In October 1979, federal minister Jake Epp (Indian Affairs and Northern Development) issued a letter, often known as the Epp letter, instructing the Commissioner to assume a role similar to that of a provincial Lieutenant-Governor, and devolving leadership of the day-to-day government to the majority leader of the legislative assembly (territorial council), to whom the Epp letter granted the authority to use the title Premier.

At that time, the government leader added a fifth elected member to the committee, which became an executive council.

Subsequent federal ministers did not revoke this authority and instruction, which was eventually codified in amendments to the Yukon Act, along with redesignation of the legislative assembly from territorial council.