The Ateneo de Manila University opened its Law School on 6 June 1936, with alumnus Manuel Lim as the first Dean. In 1939, the first graduates took the Bar Examinations, and from it emerged its first bar topnotcher in the person of Claudio M. Teehankee, who would eventually  become the Chief Justice of the Supreme Court of the Philippines in 1986.

The Ateneo Law School was closed down in 1941 as a result of the outbreak of the Second World War. The destruction of its buildings during the battle for the liberation of Manila delayed the resumption of classes after the war. In 1948, the Ateneo Law School was reopened with classes being held in the quonset huts that were erected on the ruins of the old Ateneo at Padre Faura in Manila. The Law School, since its re-opening in 1948, has produced several bar topnotchers, jurists, legislators, academicians, and noted legal practitioners.

The Law School remained at Padre Faura even as the other units of the Ateneo moved to Loyola Heights, Quezon City in January 1952. A concrete edifice was constructed in the Padre Faura campus and classes were held there until 1977.  In June 1977, the Law School transferred to a new location at the first Ateneo Professional Schools Building at 130 H.V. de la Costa, S.J. Street, Salcedo Village, Makati City. During the latter part of 1998, the Law School   transferred to its present location at the Ateneo Professional Schools (APS) Building at the Rockwell Center in Makati City, which provides for modern and spacious facilities conducive to better teaching, learning, and other academic pursuits. 

In 1986, the Ateneo Human Rights Center (AHRC), one of the first university-based institutions engaged in the promotion and protection of human rights in the Philippines, was established.  It was formally integrated into the Law School in 1996.

In 1998, the Center for Continuing Legal Education and Research was established as a special unit of the Ateneo Law School to provide continuing legal education through lecture series, legal research, and publications on relevant legal issues. The Center would later on be renamed as the “Fr. Joaquin G. Bernas, S.J. Center for Continuing Legal Education and Legal Research” when its new facility in the APS Building was inaugurated in July 2010.

In 2000, the Law School inaugurated The Chief Justice Claudio Teehankee Center  for the Rule of Law (TCRL), to serve as the Law School's research and conference center, with  books and research materials on Philippine Legal History, the Pre-Martial Law and Martial Law Periods, the United States Civil Rights Movement, the Sabah issue, Rizaliana, and International Law.

In 2004, the Ateneo Legal Services Center (ALSC) was formally established within the Law School to achieve the following objectives: (a) expand the opportunities for law students to participate in the legal aid and other related programs of the Law School by rendering service to indigent clients, thereby heightening their awareness toward alternative lawyering; (b) making justice accessible to the marginalized and indigent members of Philippine society by providing quality legal representation; and (c) offering Ateneo alumni a vehicle by which to pursue their pro bono vocation, through a closer working relationship with the Law School.

Graduates of the Ateneo Law School until 1990 were conferred the degree of Bachelor of Laws (LL.B.). Starting 1991, the degree of Juris Doctor (J.D.) was conferred on all graduates. The J.D. program is a rigid and enriched law curriculum which requires students to take both the core Bar subjects, as well as elective subjects offered to complement their knowledge of law and allow them to specialize. The program requires students to undergo a summer apprenticeship to develop the students’ appreciation of the practical and ethical aspects of law, as well as to prepare and defend a thesis.

Beginning School Year 2011-2012, the Law School formally offered to both local and foreign students the International Master of Laws Program which confers the LL.M. degree on those who comply with all the requirements mandated in the program, highlighted by the completion and successful defense of an LL.M. thesis.

The Ateneo Law School then and now continues to pursue a liberal Jesuit educational program that seeks the harmonious development of moral virtues and intellectual excellence, aimed at developing not only lawyers knowledgeable in the law and its interpretation, but also good and committed Catholic lawyers. The mold has been cast by St. Thomas More who was “the king's good servant, but God's first.”