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St. John Church began in 1888 under the sponsorship of Settle Memorial Church and the Mission Board of the Methodist Church. It was located on West Second Street and was named Main Street Methodist Episcopal Church South.
As the congregation grew and more space was needed, a new facility was completed in 1909 on the corner of West Third Street and Frayser Avenue, with a parsonage on an adjoining lot. The name was changed to Third Street Methodist Episcopal Church South.
The present facility at 2160 Griffith Avenue was constructed and completed in 1961 taking the name St. John Methodist Church. It became St. John United Methodist Church in 1968 when the Methodist Church merged with the United Brethren Church to become the United Methodist Church. The parsonage next door was purchased in 1979.
The beautiful stained glass window was also added in 1979 in memory of John Hazelrigg. The chancel area was renovated in 1989 and a prayer chapel was added in 1994 in memory of W. L. and Sylvia Wyant.
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