The origin of this body is found in the Congregatio super negotiis ecclesiasticis extraordinariis Regni Galliarum (Congregation on the Extraordinary Ecclesiastical Affairs of the Kingdom of France) that Pope Pius VI set up on 28 May 1793 to deal with problems arising for the Church as a result of the French Revolution. After the fall of Napoleon, Pope Pius VII gave it competence for negotiations with all governments about ecclesiastical matters and renamed it the Congregatio extraordinaria praeposita negotiis ecclesiasticis orbis catholici (Extraordinary Congregation in Charge of Ecclesiastical Affairs of the Catholic World). Under Pope Leo XIII, its name was shortened to Congregatio pro negotiis ecclesiasticis extraordinariis (the Congregation for Extraordinary Ecclesiastical Affairs), which remained its title even after Pope Pius X in 1909 made it part of the Secretariat of State.
This arrangement was incorporated into the 1917 Code of Canon Law, which described the Secretariat of State as composed of three sections, of which this congregation was the first:
- The Office of the Secretariat of State, presided over by the Cardinal Secretary of State, consists of three sections, in the following order:
- 1. The First Section, headed by the Secretary of the Congregation for Extraordinary Ecclesiastical Affairs, deals with the matters that must be submitted to it in accordance with canon 255, leaving other matters to specific Congregations in accordance with their different nature;
- 2. The Second Section, headed by the Substitute [i.e., Alternate Secretary of State), deals with ordinary matters;
- 3. The Third Section, headed by the Chancellor of Apostolic Briefs, deals with the despatch of Briefs.
In its canon 255, that Code defined the congregation's field of competence as erecting or dividing dioceses and appointing bishops where negotiations with civil governments were involved, and other matters that the Pope might choose to entrust to it, especially those in some linked to civil law and the Holy See's agreements and concordats with states. The Cardinal Secretary of State was concurrently prefect of the Congregation for Extraordinary Ecclesiastical Affairs with the secretary equalivant to the current secretary for Relations with States.
With the apostolic constitution Regimini Ecclesiae Universae of 15 August 1967, Pope Paul VI, following the recommendations of the Second Vatican Council, reorganized the Secretariat of State, suppressing the Chancery of Apostolic Briefs. He established what had been the First Section as a body distinct from the Secretariat of State, though closely related, and called it the Council for the Public Affairs of the Church. On 28 June 1988, Pope John Paul II issued the Apostolic Constitution Pastor Bonus, making that same body, under the name "Section for Relations with States", the second of two sections of the Secretariat of State, the first being the Section for General Affairs.