The Intergovernmental Affairs Division of the Executive is responsible for the management and development of government strategies, policies and initiatives relating to federal, provincial, territorial, circumpolar and aboriginal affairs.

It is distinctive in containing the offices of the Deputy Minister of Intergovernmental Affairs, who is also the Secretary to the Senior Personnel Secretariat. This high profile office serves the GN by participating in preparations for Intergovernmental activities such as the Western and Annual Premiers Conferences, First Ministers meetings and the Social Union Framework Agreement. It manages the Ottawa office of the GN which supports all departments in work and relationships with the Federal Government, and in the coordination and support for departmental and Ministerial meetings with Ottawa counterparts.

Under the Director of Intergovernmental Affairs the GN's role in claims and circumpolar initiatives is managed, including participation in the work of the Arctic Council, the Nunavut Implementation Panel and the Clyde River Protocol.