The Department of Finance was established in 1975. The Department reports to the Minister of Finance and has overall responsibility for the management of the Treasury, the development of fiscal policies for the GNWT and the regulation of the insurance and liquor industries. While the Department of Finance is not directly involved in the delivery of programs and services to the public, it provides support to the executive branch and program departments through the acqusition and management of financial resources.

The Treasury is responsible for managing the government's cash position, conducting the government banking and investing activities, tax administration, risk management and insurance industry regulation. Fiscal policy is reponsible for the provision research, analysis and recommendations for the fiscal policies of the government. Additionally it monitors economic conditions as they affect the government's fiscal policy including federal and NWT tax policies, intergovernmental fiscal relations and formula financing arrangements. The Department of Finance manages the sale, distribution and consumption of liquor in the NWT via the Liquor Revolving Fund, the Liquor Licensing Board, Liquor Licensing and Enforcement and the Liquor Commission.

In 2009/10 the functions of the Financial Management Board and Secretariat were transferred from the Department of the Executive back to the Department of Finance. Changes to the Financial Adminstration Act established the Minister of Finance as the Chair Financial Management Board, with the Deputy Minister of Finance becoming the Secretary of the Financial Management Board.