The federal government's legislative responsibilities for Indians and Inuit derive from section 91 (24) of the Constitution Act (1867), formerly called the British North America Act, which gives the federal government the exclusive authority to pass laws related to "Indians". The Indian Act, which remains the major expression of federal jurisdiction in this area, was passed, and a series of treaties was concluded between Canada and various Indian bands across the country. Federal jurisdiction for Indian peoples under the Constitution Act was subsequently (in 1939) interpreted by the courts to apply to Inuit as well. The Department derives its responsibilities for the North from various federal legislations.

Within this legislative framework, the Department has a number of interlocking responsibilities and objectives. The Department's principal emphasis is on pursuing initiatives to assist First Nation communities to overcome obstacles to their development and to help them marshal the human and physical resources necessary to build and sustain viable communities. Particular focus is on negotiating First Nations governance, settling land claims, supporting the development of communities to improve on‑reserve economic opportunities and living conditions, including their environmental health and safety situations, achieving the transfer of provincial-type responsibilities to the territorial governments, and promoting northern environmental awareness and sustainable development. Increasingly, the Department is devolving its powers and responsibilities to the First Nation peoples and territorial governments directly concerned.

The department also supports the Minister in his role as Federal Interlocutor for Métis and Non-Status Indians – serving as the focal point of contact between the Government of Canada and aboriginal organizations representing Métis, Non-Status Indians and urban Aboriginals. On June 1^st, 2008, the former department of Indian Residential Schools Resolution Canada was amalgamated with the department. The new Resolution Sector is responsible for addressing and resolving issues arising from the legacy of Indian Residential Schools including effective implementation of the Indian Residential Schools, Settlement Agreement approved by the Courts.

Finally, in the context of its responsibilities in the North, the department provides leadership in supporting northern political and economic development, including implementing the Government's vision for a new North that will protect and secure Canada's sovereignty and create more economic opportunities.