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The Parish of St. John's had its earliest beginnings as Grace Church in 1854, served by seminarians. In 1865, it was reorganized as St John's, when the Rev. Dr. James McCook became its first rector. The church building was consecrated on June 22, 1869.

In 1909 the Vestry voted to accept the offer of Miss Mary Coming to construct a building to be used for recreational and community purposes. Shortly thereafter Corning Hall was build. It is located at 12 Rector Street, behind the church building. No longer needed as a recreational building, it was remodeled in the 1970's to meet the needs as a parish hall and community meeting center.

Dr. McCook was succeeded as Rector by the Rev. James W. Lord in 1927, who served until 1951. He was succeeded by the Rev. Shennan W. Andrews who served as rector until 1965. Under his leadership, All Saints' Mission was established on Hills Street in the South end of town. The Rev. John Hays Duff became rector in 1965, serving until 1972. The Rev. Alva G. Decker became rector in 1973 and served until 1982. During his tenure, the Parish struggled with its changing neighborhood and its ministry to those changed circumstances. 

The Rev. William F. Loutrel became the sixth Rector of St. John's in March of 1984. Under his leadership, the Parish worked to strengthen its mission and ministry in the world through a process of parish development, improved stewardship, increased lay leadership, and pastoral care by both clergy and laity. Father Loutrel served until May 14, 1989.

On All Saints' Day, November 1, 1990 the Parish took a bold, creative step in a new direction. On that occasion the Greater Hartford Regional Ministry (GHRM) came into being when, in the presence of the Bishop, the Charter (Covenant) of this new ecclesial venture was signed by the wardens of the participating parishes. The Greater Hartford Regional Ministry brought together four Episcopal parishes (All Saints', East Hartford; St. George's, Bolton; St. James', Hartford; and St. John's, East Hartford) in an intentional and co-operative relationship, in which significant resources and talents were shared. Instead of the one-priest, one parish model of church, GHRM had a clergy team that rotated among the parishes. This team was guided by the Missioner, the Rev. Thomas C. Ely. All the major feast days of our Lord were celebrated as joint liturgies on the day they occurred. Adult education was done jointly. The focus and thrust of GHRM was on Total Common Ministry.

Ultimately, after 21 years of Total Common Ministry, the cluster was dissolved and the churches reverted to their individual status.

As of Sunday, January 1, 2017, St. John's Episcopal Church, East Hartford joined the Episcopal parish of St. John's Church, Vernon. The people of St. John's, Vernon warmly welcomed their fellow Episcopalians and the people of the former St. John's moved into leadership roles within their new home. The heart of the Episcopal community is in its worship, as they gather week after week to be fed at the Lord 's Table. Strengthened by the sacraments, informed by God's word, and empowered by the Holy Spirit, they continue to reach out in love and concern for others.