The original organ was a rebuilding by George Andrews of an older G-compass organ, very likely by Alvinza Andrews. The 5-section case is identical to a stock design of the elder Andrews originally installed in Frankfort, NY, later Worcester, NY, and as of 2020 recently relocated to the former Presbyterian Church in Vernon Center, NY.

Andrews the younger converted the organ to C-compass, simply blocking off the lowest 4 notes of the older windchest; added additional stops, enclosed the organ behind shutters, and added a 13-note pedal division.

The organ was originally installed in the gallery, later moved to the right front of the church when the building was modified with the addition of a chancel, and installed against the right-front wall. The church was originally affiliated with St. John's Academy and located on the school grounds. In the 1880s this became the Manlius Military Academy, merging with the Peeble Hill School in 1970. The older campus was closed in 1974 and in 1979 the school buildings were renovated to became the Manlius School Apartments.

Howard Marsh, one of the original employees of the Schlicker Organ Co., was for many years an organ instructor at SUNY Fredonia, becoming Dean of the Music Department in 1973, and Dean of the School of Fine Arts in 1975. Long-time best friends with a member of the Manlius church, Marsh was given the task in 1975 of restoring and enlarging the instrument to make it musically current. He would do the work on weekends, and hire students from the Fredonia Music Dept. to assist, including this author at the end of the project in the summer of 1976. Marsh's work included the following:

• cleaning of the organ and pipework
• replacement of the double-rise reservoir with a Schlicker floating-top reservoir
• replacement of the Spencer blower with a new silent Ventus unit
• replacement of the 13-note pedalboard with one of larger compass, and extension of the 13-note Bourdon to full compass with spurious antique pipework
• removal of the center 3 flats (of 5 total) of half-round gilded wooden dummies, with acoustically transparent grill cloth
• installation of slide tuners on the open metal pipes, and repitching the organ to A440
• replacement of the original Dulciana (tenor-c) with a Twelfth of new tin pipes from Schlicker
• the visibile casework, previously painted white over the original faux graining, was left untouched

In 1997, the church interior was "modernized" and the organ was thoughtlessly discarded and replaced with an imitation machine. The organ was acquired by Jeremy Cooper through the Organ Clearing House, and has been installed in a church in New Hampshire, heavily altered.