Prior to the installation of a pipe organ, a seraphine and then a harmonium were used for musical accompaniment.
 The first organ was installed above the gallery at the western end of the church by William Davidson at the request of the rector J. C. Corlette, and was transferred to the south transept in about 1879, where it remained until 1882 when it was sold to St Bartholomew's, Pyrmont, and later St Luke's, Northmead.

The 1883 Hill and Son organ, including 844 pipes, costing a total of £550, was installed in 1884, and located in the north-east corner of the transept.
It is still in use, with original pipework, making it faithful to the original tones.
The organ was refurbished and rebuilt in 1950, 1975, and 2008.

The 1950 change from mechanical to electrical action was motivated by removing the increasingly noisy pedals and trackers.
This refurbishment also included detachment of the console (to the other side of the transept), and replacement of the bellows with a "pressure equaliser".
The façade pipes were sprayed to a dull gold colour, covering over the original diapering, described disparagingly at the time as "all over the pipes without much rhyme or reason; fleurs-de-lys in profusion, dots, bands, triangles in all the colours of the rainbow rioted in confusion".
 This work was carried out by R. A. and D. A. Wiltshire.

By 1975 the organ had become unplayable, and a reconversion to mechanical action was undertaken.
 The console was moved back to the organ side of the transept, with the action going backward under the floor into the organ.
 This necessitated removal of floor joists and foundation piers, but the unsupported floor caused further problems long term, and during the 2008 rebuild it was re-electrified.

Between 2006–2008 Sydney firm "John W Parker – Pipe Organ Builders" refurbished the organ, returning the soundboard action to electric, providing a new roll-top 'detached' console, and an entirely new wind supply and bellows.
The swell box which had been discarded in the 1975 rebuild was reinstated, and the pedal Bourdon 16' stop was extended to 8' pitch.
Octave couplers were provided in Sub and Octave pitches on the Swell also.
All manual pipework was washed, cleaned and regulated to original Hill standards and tonality.

The church had a significant choral history, with significant events often celebrated with a full choir, sometimes accompanied by an orchestra.
In the late 19th century the St John's choir participated in regional choir festivals.
Prior to the installation of a pipe organ, a seraphine and then a harmonium were used for musical accompaniment.  The first organ was installed above the gallery at the western end of the church by William Davidson at the request of the rector J. C. Corlette, and was transferred to the south transept in about 1879, where it remained until 1882 when it was sold to St Bartholomew's, Pyrmont, and later St Luke's, Northmead.
The 1883 Hill and Son organ, including 844 pipes, costing a total of £550, was installed in 1884, and located in the north-east corner of the transept. It is still in use, with original pipework, making it faithful to the original tones. The organ was refurbished and rebuilt in 1950, 1975, and 2008.
The 1950 change from mechanical to electrical action was motivated by removing the increasingly noisy pedals and trackers. This refurbishment also included detachment of the console (to the other side of the transept), and replacement of the bellows with a "pressure equaliser". The façade pipes were sprayed to a dull gold colour, covering over the original diapering, described disparagingly at the time as "all over the pipes without much rhyme or reason; fleurs-de-lys in profusion, dots, bands, triangles in all the colours of the rainbow rioted in confusion".  This work was carried out by R. A. and D. A. Wiltshire.
By 1975 the organ had become unplayable, and a reconversion to mechanical action was undertaken.  The console was moved back to the organ side of the transept, with the action going backward under the floor into the organ.  This necessitated removal of floor joists and foundation piers, but the unsupported floor caused further problems long term, and during the 2008 rebuild it was re-electrified.
Between 2006–2008 Sydney firm "John W Parker – Pipe Organ Builders" refurbished the organ, returning the soundboard action to electric, providing a new roll-top 'detached' console, and an entirely new wind supply and bellows. The swell box which had been discarded in the 1975 rebuild was reinstated, and the pedal Bourdon 16' stop was extended to 8' pitch. Octave couplers were provided in Sub and Octave pitches on the Swell also. All manual pipework was washed, cleaned and regulated to original Hill standards and tonality.
The church had a significant choral history, with significant events often celebrated with a full choir, sometimes accompanied by an orchestra. In the late 19th century the St John's choir participated in regional choir festivals.
St John's, Ashfield