Its principal responsibility is the administration of Inuit lands and the over CAN$120 million in compensation funds it has received under the terms of the James Bay and Northern Quebec Agreement of 1975. It has a mandate to use those funds to promote the economic and social development of Inuit society in Nunavik. The Makivik Corporation is also empowered to negotiate new agreements with governments on behalf of the Quebec Inuit and to represent them on bodies like the Inuit Tapiriit Kanatami and the Inuit Circumpolar Council.
The corporation is run by a five member executive committee including a president, and an 16 member board of directors. Members of both bodies are elected by the Inuit of Nunavik. The executive committee and board of directors together appoint a board of governors to act as an elder's council. Makivik's current president is Pita Aatami. It is headquartered in Kuujjuaq, Quebec, and has offices in Inukjuak, Montreal, Quebec City, and Ottawa. It has roughly 100 employees.
Makivik has donated some CAN$60 million to non-profit and cultural institutions in Nunavik, including funding the construction of recreation facilities in each of Nunavik's communities. However, the bulk of its financial activities have been in the form of investments, both in Canadian and international markets and in economic activities directly relevant to Nunavik. It has a number of wholly owned subsidiaries and joint ventures active in Nunavik: