[14] The new campus started functioning on 1 August 1974 at the Parameswara College premises in Thirunelvely some 4 km north of Jaffna city centre.

The Faculty of Science was based at the undergraduate section of Jaffna College, Vaddukoddai which had been taken over by the government on 13 August 1974.

Construction of a new library, student centre and arts block began in 1981 but were halted due to the civil war.

The escalation of hostilities between the Indian Peace Keeping Force and the rebel Liberation Tigers of Tamil Eelam in late 1987 severely affected the university.

[14] During the late 1980s/early 1990s, when most of the Jaffna peninsula including Jaffna city was under LTTE control, the university suffered frequent aerial bombings, shortage of essential goods due to the economic blockade, shortage of academic staff many of whom had fled abroad and a general disturbance of academic life due to the frequent curfews.

The university's administration returned to Thirunelvely in 1996 after the military had recaptured most of the peninsula including Jaffna city.

[14] Construction of a new building for the Faculty of Agriculture at Ariviyal Nagar, Kilinochchi began after the end of the civil war in 2009.

[16] The university is based at five sites: Thirunelvely, Vavuniya, Ariviyal Nagar, Kaithady and Maruthanarmadam.

The Faculty of Graduate Studies is based in a rented house on Ramanathan Road opposite the university.

The faculties of Agriculture, Engineering and Technology are based at Ariviyal Nagar near Murukandy, south of Kilinochchi.

[15] Construction of a new building for the faculty at Ariviyal Nagar, Kilinochch began after the end of the civil war in 2009.

[15] This building complex was renovated with the state fund and Faculty of Agriculture started to function in that place since December 2014.

The faculty has established crop and livestock farms in Ariviyal Nagar, Kilinochchi to provide a sound practical training in Agriculture to the students.

To support the academic programmes as well as the outreach activities, the Faculty has absorbed an Integrated Farm and Training center located at Puliyankulum.

Meantime a skill development center consisting of Conference hall, Computer unit, Library, Canteen and student complex was built with the financial support of the Government of India.

A full-fledged Research and Training Complex has been established with the support of Japan International Cooperation Agency (JICA) in 2021.

In 2003, the UGC invited discussions on the introduction of six Allied Health Sciences (AHS) degree programs in Sri Lankan universities.

The UAHS faced challenges such as increased student intake and infrastructure limitations, but efforts were made to improve facilities and resources.

The annual student intake was increased, and plans were made to construct a state-of-the-art building to accommodate the growing needs of the faculty.

The faculty continues to face challenges related to student accommodation and laboratory facilities, but efforts are underway to address these issues.

The Faculty of Applied Sciences was established when the Vavuniya Campus of the University of Jaffna was created in April 1997.

[14] K. Indrapala, senior lecturer in history at the Peradeniya Campus of the University of Sri Lanka, was appointed the first Dean of the Faculty of Humanities.

[29] Eight new departments were created: Sanskrit (1975),[30] Education (1980),[29] Language and Cultural Studies (1981),[31] Fine Arts (1982),[32] Economics, Geography, Islamic Civilization and Philosophy.

[31][33] The Department of Siddha Medicine was removed from the faculty in October 1993 and now functions directly under the control of the vice chancellor.

[10][23] The Faculty of Business Studies was established when the Vavuniya Campus of the University of Jaffna was created in April 1997.

[14][57] P. Kanagasabapathy, Head of the Department of Mathematics at the Peradeniya Campus of the University of Sri Lanka, was appointed the first dean of the Faculty of Science.

[58][59] The facilities at Jaffna College proved to be inadequate and construction of a new building for the faculty at the Thirunelveli site began in 1975.

[57] The faculty left Jaffna College and moved into the Natural Science Block at Thirunelveli in June 1978.

The foundation for the building to the Department of Computer Science was laid on June 27, 2019 with the World Bank-funded AHEAD operations.

[24] The faculty offers undergraduate courses which lead to Bachelor of Information Communication Technology Honours (BICT Hons.)