Founded in 1822, St. James was the first Catholic church on Long Island and thus the cradle of Catholic Christianity for two dioceses and 388 parishes.
The parish of Saint James was the third parish to be erected within the present confines of New York City, being predated only by St. Peter's on Barclay Street and Old Saint Patrick Cathedral, both located in lower Manhattan. Saint James was constructed in response to the request of 70 laymen who petitioned for a parish in Brooklyn. The sentiments of the first parishioners are captured well in a circular letter sent by Peter Turner to his fellow Catholics:
"In the first place, we want our children instructed in the principles of Holy Religion, we want more convenience in hearing the Word of God ourselves. In fact, we want a Church, a Pastor, and a place of Interment."
The site of the first cemetery on Long Island was established at Saint James. There were nearly 7,000 burials between 1823 and 1849.
In 1853, upon the creation of the Diocese of Brooklyn, Saint James became the Cathedral parish of the Diocese. The original parish church of Saint James, which was severely damaged by a series of fires, was replaced in 1903 by the existing church building under the direction of the second Bishop of Brooklyn, Charles McDonnell. Bishop McDonnell also introduced the term "Pro-Cathedral" in light of his plans to build the Cathedral of the Immaculate Conception in Fort Greene, on the present site of Queen of All Saints and Bishop Loughlin High School.
In 1972, on the occasion of the 150th anniversary of Saint James, Bishop Francis Mugavero, the fifth Bishop of Brooklyn, proclaimed Saint James as the "Cathedral" of the Diocese of Brooklyn, thereby restoring the title given by Bishop Loughlin, the first Bishop of Brooklyn.
In 1979, during Pope Saint John Paul II's first Apostolic visit to the United States of America, the Holy Father made an unforeseen visit to the Cathedral and greeted the parishioners gathered on Jay Street.
In 1982, on the occasion of the 160th anniversary of the parish, Saint James Cathedral was elevated to a Minor Papal Basilica. Henceforth, the diocesan church of Brooklyn and Queens is titled "The Cathedral Basilica of Saint James."