It managed the territory of the James Bay and Northern Quebec Agreement between the 49th and 55th parallel, with the exception of the Cree Category 1 lands and the enclaves of Chapais, Chibougamau, Lebel-sur-Quévillon and Matagami.

It became a municipality of a special type directed by the mayors of the four enclave towns, as well as the chairpersons of the local community councils of Radisson, Valcanton and Villebois.

The Regional government covers a territory comprising all lands of Jamésie (TE) minus the four local municipalities (municipalité locale) — also known as the enclosed municipalities' — of Chibougamau, Lebel-sur-Quévillon, Chapais, and Matagami, and eight of the nine Cree communities (communautés crie) of Eeyou Istchee TE.

[12] Eeyou Istchee James Bay forms part of the federal electoral district of Abitibi—Baie-James—Nunavik—Eeyou and has been represented by Sylvie Bérubé of the Bloc Québécois since 2019.

Provincially, Eeyou Istchee James Bay is part of the Ungava electoral district and is represented by Denis Lamothe of the Coalition Avenir Québec since 2018.