The Cultural Endowment is directed by a supervisory board of eleven members, including the Minister of Culture as chairman, a representative designated by the Minister of Culture, a representative designated by the Minister of Finance, and 8 representatives designated by each endowment panel. The term of authority of the supervisory board is two years. The membership of the supervisory board shall be approved by the Government of the Republic.

The supervisory board of the Cultural Endowment shall:

• establish the procedure for the investment of assets of the Cultural Endowment and for entry into other transactions, and prescribe limitations on the management of the financial risks relating to the types of assets, currency structure, duration of instruments and investments, and other investment indicators;
•  distribute annual revenue pursuant to subsection 3 of § 4¹ of this Act;
• decide on financing cross-disciplinary cultural projects and projects initiated by endowments and expert groups;
• allocate the amounts intended for cultural buildings pursuant to the Gambling Tax Act according to the ranking of the construction and renovation of cultural buildings which are of national importance, which is approved by a resolution of the Riigikogu;
• determine limitations on the amount of grants and fees for creative work per year and per quarter awarded by the endowments and expert groups;
• analyse the results of the activities of the expert groups, endowments and of the Cultural Endowment;
• organise the publication of annual overviews of the activities of the Cultural Endowment;
• hire and release internal auditors of the Cultural Endowment;
• pass the annual budget, approve the financial plan and audited annual report of the Cultural Endowment;
• determine a separate budget prescribed for an internal audit in the funds prescribed for the administrative expenses of the Cultural Endowment and approve the work schedule of internal auditors;
• determine the amount of remuneration to be paid to members of the endowment panels and members of expert groups and the procedure for payment thereof;
• approve the structure of the Cultural Endowment;
• appoint to and release from office the Director of the Cultural Endowment;
• exercise supervision over the activities of the Director, endowments and expert groups;
• make proposals and express opinions concerning other issues involving the development of the arts, folk art, physical fitness and sport and relating to the performance of functions provided for in this Act;
• select an asset manager set out in subsection 1 of § 6¹ of this Act and approve the conditions of the agreement to be entered into with the asset manager;
• decide, on the proposal of the Director, the acquisition and transfer of immovables.