• Msgr. John B. Sullivan, July 1, 1914-June 30, 1959
• Msgr. Charles v. Boyle, June 30, 1959-1973
• Fr. James Boyle / Fr. John Mulligan, Feb. 15, 1973-June 1981 [Co-pastorate]
• Fr. Peter Clifford / Fr. Kevin Murphy, June 1981-June 25, 1991 [Co-pastorate]
• Fr. Kevin Murphy, June 25, 1991-June 25, 1996 [sole pastor]
• Fr. William V. Spilly, June 25, 1996-2004
• Anne-Marie Brogan, Sep. 2001-Dec. 2001 [Temporary administrator, sabbatical]
• Fr. Robert J. Schraeder, June 29, 2004-June 29, 2021 [Upon retirement]
• Fr. Peter B. Mottola, June 29, 2021-present

In early 1914, Bp. Thomas Hickey made the decision to establish a new parish in the northern section of Brighton (which would later become part of the City of Rochester in 1922). The parish began with 68 families from Corpus Christi, Blessed Sacrament, Our Lady of Victory, and St. Joseph. Fr. John B. Sullivan was assigned as the founding Pastor, and the parish was formed on July 1, 1914. Work quickly began on building up this new parish. Ground was broken for a combination church/school building on Sep. 20, 1914. The cornerstone was laid Oct. 4, 1914 in a grand ceremony presided over by Bp. Hickey. The first church was completed by 1916 at a cost of $35,000. The church was on the first floor, four classrooms were on the second, and an auditorium was in the basement. The school was staffed by the Sisters of Mercy who resided at the Our Lady of Mt. Carmel convent until a new convent was completed at 340 N. Winton Rd in 1922.

The parish grew rapidly during the 1910s and early 1920s, which led Fr. Sullivan to draw up plans for a new church building. Original aspirations for a basilicaesque structure with transepts had to be curtailed due to a lack of funds. The desired 750-seat church ended up with a much smaller capacity of 500, and a smaller sanctuary than intended. The new church would have an array of impressive, large stained glass windows designed by Norman Lindler and Herman J. Butler, and created by James O'Hara and Pike Stained Glass Studio.

Growth continued during the pastorate of Fr. Sullivan. In honor of his achivements as Pastor, Fr. Sullivan was raied to the rank of monsignor on Oct. 8, 1949. Msgr. Sullivan oversaw additional projects in the 1950s, such as the construction of a new rectory in 1952 and a new convent in 1955. The organ, still in use today, would be installed by the Tellers company in 1953. Msgr. Sullivan's final achievement as founding Pastor was the completion of a new 16-classroom school building in 1959. He would retire that same year.

Msgr. Charles v. Boyle assumed the pastorate on June 30, 1959, following the 45 year tenure of Msgr. Sullivan. The new school building would be dedicated in 1960. The parish would eventually begin to suffer financial difficulties, with a debt of $35,000, and have to face numerous repairs to the parish's stained glass windows (55 holes were present in the large stained glass).

On Feb. 15, 1973, Frs. James Boyle and John Mulligan were appointed as one of the earliest co-pastorates in the Diocese of Rochester. The parish began holding Bingo nights to help offset the cost of needed repairs and get the parish out of debt. In 1976, a renovation committee was formed, and the sanctuary was altered so that the altar was moved out into the nave with a daily Mass chapel constructed in place of the former sanctuary and the two side altars removed. Parishioners were divided by this move, and modifications were made to the new layout by architect Robert Macon. Other modifications included an expanded parking lot and new entrance to the church.

During his first year in Rochester, Bishop Matthew Clark resided at the St. John rectory with his priest secretary, Fr. Charles Latus. After about a year, Bp. Clark would move into the rectory at Sacred Heart Cathedral. In June of 1981, another team of co-Pastors would be appointed to lead the parish, Frs. Peter Clifford and Kevin Murphy. Following the departure of Fr. Clifford in 1991, Fr. Murphy continued on as the sole Pastor. Beautification projects would take place during this period, such as the addition of a Peace Garden in 1992 by Fr. Zimmer, a new parking lot entrance in 1994, and a repainting and recarpeting of the church in 1996.

St. John the Evangelist would form a collaborative partnership with neighboring parishes, St. Ambrose and St. James, in 2004 as the "Winton-Culver Catholic Community" in response to diocesan pastoral planning. This arrangement would eventually lead to formation of a unified three-site parish on May 18, 2007 called "Peace of Christ." St. John's school would close in June 2005.

St. John continues as part of the Peace of Christ parish to this day, and is presently led by Fr. Robert Schraeder.