At a St. Francis Parish meeting in October, 1880, it was decided to build a parochial school to serve the predominatly Irish Catholic Fair Haven Community. This decision was reached only twelve years after the construction of St. Francis Church. Parishioners sought to assure that their children would receive a thorough education in their Catholic faith.

When the school opened in September, 1881, with an enrollment of 700 students, it was staffed by the Sisters of Mercy of the Hartford Diocese. The relationship between the Sisters of Mercy and St. Francis School was to endure for over 100 years.

Throughout the years, the school underwent numerous additions and renovations. In 1923, classrooms were added to the four story structure. Major renovations in 1950, included the removal of the fourth floor, the addition of fireproofed interior stairwells, the installation of modern lavatory facilities, an imporved heating system and new classroom flooring.

The school provided a half-day Kindergarten program at least as early as the 1930's. For a period of five years beginning in 1961, a ninth grade was offered to students who wished to remain largely because of the K-6, 7-9, 10-12 grade organization of the New Haven Public Schools. The Sister Clara, RSM library was opened in 1961, in part, to serve the expanded demands necessitated by the ninth grade. The Pre-Kindergarten classroom opened in 1989-1990, followed by an afterschool program in 1991-1992.

After 104 years of continuous, exceptional service to the children of Fair Haven, the Sisters of Mercy closed their convent adjacent to the school in 1985. With the resignation of Sister Sheila Durante, RSM, the school was required to operate without the guiding infulence of its primary teaching order. In the fall of 1985, Sister Julianna Poole, SSND, took on the position of school prinicpal. At the time, she was the only religious on staff. An unusually perceptive professional, Sr. Julianna chronicled her observation of St. Francis School in a comprehensive presentation to the United States Office of Education, successfully nominating St. Francis to become one of the initial 60 private schools nationwide to receive the Excellence in Education Award.

In 1988, George Kelly became the first layman to serve as principal of St. Francis School. On his retirement in 1991, he was succeeded by Robert Schreck, PhD., a member of the St. Francis School Class of 1948. Dr. Schreck is the first lay graduate to serve as principal. Concurrent with his arrival, the faculty was bolstered by the addition of three religious; two Sisters of Mercy and a Dominican Sister of Hope. In 1999, Mr. Frank Smith became the principal of the school. In 2005, Dennis Beaupre succeeded Frank Smith. Principal Victor Vessicchio, a 1964 graduate of St. Francis School, succeeded Frank Smith in 2008, until 2016, when Mrs. Taryn Duncan became principal.

The school is ever alert to the needs of its children and their families. The school has activiely sought volunteer tutors and has developed an extensive collaboration with Quinnipiac University. This arrangement has resulted in numerous class trips to the Quinnipiac campus and numbers of Quinnipiac students servicing as school volunteers. Through the efforts of the school, numerous educational and recreational programs are made available to students during the summer.

As the early years of the 21st century begin, the histroy of St. Francis continues to be written. The history combines the rich heritage of the past with a bright view of the future.