The Council of Parties is the organ of the Centre where the Parties to the agreement are represented, with the Holy See attending as Founding Observer. The Council convenes at least once a year. Its functions include the election of members of the Board of Directors and the appointment of the Secretary-General and Deputy Secretary-General.

The Council of Parties adopts the Centre’s financial regulations, work programme and annual budget. The Council of Parties also, on the basis of proposals of the Board of Directors, nominates the members of major religions and faith-based and cultural institutions to the Advisory Forum. It will approve international agreements and will approve the establishment of cooperative relationships with public or private entities that can contribute to the Centre’s work. The Council of Parties will decide on the admission of new parties and observers to the Agreement.