In January 1825, members of Old South, Park Street, and Union Churches met to plan a meetinghouse to serve the Northern section of Boston. This meetinghouse came to be Hanover Street Church, which was dedicated and opened its doors on March 1st, 1826. Reverend Lyman Beecher was installed as pastor on the 21st of that month, after having formerly worked assisting the pastors of Old South, Park Street, and Union Churches.

In 1830, Henry Ward Beecher was admitted to be a member of the church. On February 1st of that same year, the original meeting house burned down. It was decided to move the church from the North End to Beacon Hill, leading to the opening of the house of worship for the Bowdoin Street Church on May 15th, 1831. On September 26th, 1832, Reverend Lyman Beecher was dismissed from his position as pastor after answering the call to take charge of Lane Theological Seminary in Ohio. That same day, Reverend Hubbard Winslow was installed in his place.

Reverend Edwin Johnson was installed as pastor in June 1859. He served at Bowdoin Street Church until his resignation in September 1861 after declines in membership led him to look elsewhere. He then answered the call to serve Hammond Street Church in Bangor, Maine. On December 13th of that year, the meetinghouse of the church was put up for sale in an auction.

By June 17th, 1863, the meetinghouse was sold to the Church of the Advent and the Bowdoin Street Church was dissolved. In 1883, it was sold to the monastic order known as the Society of St. John the Evangelist and became the Mission Church of St. John the Evangelist. Since 1985, it has served as a Parish Church in the Episcopal Diocese of Massachusetts.