After the opening of St. John's College in 1867, most minor seminarians for the Diocese of Saint Paul were educated there or at other seminary institutions in the United States or in Europe.

[1] Grace's successor, John Ireland, took office in June 1884, and in December of that same year announced plans to build a seminary for the diocese, which would become the College of St. Thomas.

Ireland's primary benefactor for this project was James J. Hill, president of the Great Northern Railway.

John Ireland's deep involvement with the Catholic University of America led to an affiliation that allowed any graduate of SPS to present himself for a baccelaureate degree from CUA.

With the additional assignment of an axuliary bishop for Saint Paul, six priests required episcopal consecration.

However, due to declining enrollment after the Second Vatican Council, by 1967 the "4-4-4" plan seemed no longer feasible and there was a stronger desire to create a college seminary at the University of St. Thomas and close Nazareth Hall.

While the Saint Paul Seminary and University of St. Thomas both were owned by the archdiocese and were next to each, they operated separately.

The Ireland library building was included in the sale, but the books remained the property of Saint Paul Seminary.

During his tenure as rector, Saint Paul Seminary greatly increased its enrollment and programs.

On January 1, 2019, Joseph Taphorn succeeded Callaghan as Saint Paul Seminary rector.

Classes are held in the Brady Educational Center, which also houses the undergraduate music department of the University of St. Thomas.

Loras, Grace, and Cretin halls were the original SPS residence buildings; they were sold to the University of St. Thomas during the seminary/university affiliation agreement.

The cornerstone of the chapel was laid during a Pontifical Mass on July 2, 1901, the fiftieth anniversary of Bishop Joseph Crétin's arrival in the new diocese.

Bishop Fulton Sheen, in his autobiography A Treasure in Clay, talks about how his love for a daily Holy Hour was started at St. Mary's Chapel.

The chapel was renovated in 1988, as part of the construction of the new SPS building, with a new design by Frank Kacmarcik which included reversing the interior of the chapel, removing the statues from the side altars, and removing or updating many components of the interior decoration.

As of the 2022–2023 academic year, SPS had 82 seminarians in formation for the priesthood, representing 16 dioceses and religious communities.

[6] Seminarians participate in a wide variety of activities, including choir, schola, theatre, and sports.

While most of the productions have only been put on by seminarians from SPS, Saint John Vianney College Seminary has been invited to join some of them as well.