The Jay Phillips Center was established in 1996 as the  Jay Phillips Center for Jewish-Christian Learning by bringing together Saint John’s University’s Jay Phillips Chair in Jewish Studies and the University of St. Thomas’ Center for Jewish-Christian Learning.

The Jay Phillips Chair in Jewish Studies, named after the Jewish philanthropist who endowed it, was established in 1969 upon the recommendation of Fr. Colman Barry, president of Saint John's University from 1964 to 1971.  Rabbi Nahum Schulman served as the chair’s first occupant until 1983, followed by Rabbi Michael Goldberg (from 1983 to 1985), Rabbi Mark Verman (from 1987 to 1993), and Rabbi Barry D. Cytron (from 1996 to 2009).  A national search for a new occupant of the chair will be conducted in the near future.
The Center for Jewish-Christian Learning, endowed by a number of Jewish and Catholic benefactors led by Sidney R. Cohen and Thomas P. Coughlan, was established in1985 upon the recommendation of Msgr. Terrence J. Murphy, president of the University of St. Thomas from 1966 to 1991.  Rabbi Max A. Shapiro served as the center’s director from its beginning until his retirement in 1996.

Arthur E. Zannoni served as the center’s associate director from 1985 to 1991, followed by Karen L. Schierman who continued in that role after the 1996 reconfiguration and renaming of the center.  Among his many services to the center, Zannoni edited the first seven volumes of the Proceedings of the Center for Jewish-Christian Learning.  SrMary Christine Athans, B.V.M., professor emerita of church history at The Saint Paul Seminary School of Divinity, was closely associated with the center from its beginning, and she served as editor of volumes eight to eleven of the center's Proceedings.

Under Rabbi Shapiro’s guidance and upon the recommendation of Fr. Dennis Dease, president of the University of St. Thomas from 1991 to 2013, and Br. Dietrich Reinhart OSB, president of Saint John's University from 1991 to 2008, the collaboration between the University of St. Thomas and Saint John’s University brought about the jointly sponsored Jay Phillips Center for Jewish-Christian Learning in 1996.  Rabbi Barry D. Cytron served as the center’s director while also holding the Jay Phillips Chair in Jewish Studies until his retirement in January 2009.  Throughout Rabbi Cytron’s tenure as the center’s director, John Merkle and Karen Schierman served as associate directors of the center.

Under Rabbi Cytron’s leadership, the center began to extend the scope of its interfaith work beyond Jewish-Christian relations.  In 2007 Rabbi Amy Eilberg became a consultant to the center and initiated its Interfaith Conversations Project to engage adult members of Christian, Jewish, and Muslim congregations in interfaith learning and activities.

At the request of Edward Phillips and Dean Phillips, grandson and great grandson respectively of Jay Phillips, and upon the recommendation of Fr. Dennis Dease, president of University of St. Thomas from 1991 to 2013, and Fr. Robert Koopmann OSB, president of Saint John’s University from 2009 to 2012, in 2009 the center expanded its mission to promote interfaith learning among people of various religions and was given its new name to reflect its expanded mission. 

In February 2009 John Merkle was appointed interim director of the center and in August 2009 he was appointed the center’s director.  Karen Schierman continued in her role as the center’s associate director until her retirement in May 2010.  In June 2010 Lois Dament became the center's administrative assistant at St. Thomas, Carol Johannes assumed the same role at Saint John's, and David Jordan Harris became the center's interfaith arts special consultant.  After winding down her Interfaith Conversations Project in June 2011, Rabbi Amy Eilberg became the center's special consultant for interfaith conversations beginning July 2011.  In June 2011 Hans Gustafson became the center’s assistant director and in June 2013 was named its associate director.