The Australian National University Act 1946 establishes the Council as the governing authority of the University. The Interim Council dates from 1 August 1946 to 30 June 1951. From 1 July 1951 the term Council was used. Its membership was provided for by section 11 of the Act including members elected by the Senate, the House of Representatives, the Governor-General, Convocation, students and staff and co-opted members. It is chaired by the Chancellor and the Vice-Chancellor is also a member. Amendments to the Act in 1960 increased its members to include the Pro-Chancellor, the Deputy Vice-Chancellor, the Principal of the School of General Studies, and the Deputy Chairman of the Board of the Institute of Advanced Studies.

The Advisers on Legislation was a committee responsible for advising the Australian National University Council on university legislation and statutes. It was initially chaired by Professor (later Sir) Kenneth Bailey and its early members included the Vice-Chancellor, H F E Whitlam (Commonwealth Solicitor-General) and Sir Robert Garran.

The Standing Committee of the Australian National University Council was provided for by section 24 of the Australian National University Act 1946 and was delegated with the authority for much of the routine management of the University. It was appointed in 1951, first meeting on 13 July that year. The Vice-Chancellor originally chaired the meetings but from 1971 the Act was amended and the Pro-Chancellor took on this role. Its membership of 7-9 Council members was largely of University officers. The Act was further amended in 1991, removing reference to the Standing Committee, although it continued to meet less frequently until June 2000.

The Professorial Board was established by amendments to the Australian National University Act in 1960 as an advisory body to Council on any matter relating to education, learning or research. It was chaired by the Vice-Chancellor and all professors of the University were members. As the other two Boards, the Board of the Institute of Advanced Studies and the Board of the School of General Studies (later The Faculties), were identified as being responsible for all academic matters relating to their bodies, the role of the Professorial Board was unclear. Section 15D of the Act provides that the Vice-Chancellor 'may at any time convene a meeting' and 'shall convene such a meeting' if required by the Council, either of the other two Boards, or six members of the Professorial Board. It had its first meeting on 30 September 1969, met rarely and had its last meeting on 12 April 1989.

The first meeting of the Degree Committee was held on 10 May 1956. The Degree Committee reported to the Board of Graduate Studies up until September 1960, and from October 1960 to the Board of the Institute of Advanced Studies.

The Board of Graduate Studies provided guidance and advice to the Australian National University Council on all matters of academic policy and practice relating to education, learning and research. It was provided for by section 22 of the Australian National University Act 1946 and statute 4 of 1950. This statute was repealed by statute 36 in 1960. It first met on 4 December 1950 and was chaired by the Vice-Chancellor. Its members were Professors of the University, the Registrar, the Librarian and from 1956 the Master of University House. Its last meeting was on 23 September 1960 and it was effectively replaced by the Board of the Institute of Advanced Studies.