During Edward Judson's time, the Church sponsored a weekly singing class for the Italian immigrants of the South Village, and, for a time, employed one of the musical Damrosches as the teacher. The church Meeting Room's vibrant acoustics have enhanced many concerts by guest artists, from Mahalia Jackson in the 1950s to Arcade Fire in 2007 and Alanis Morissette and Steve Earle in 2008.

Judson was briefly associated with the folk singing movement in the early 1960s when City Parks Commissioner Newbold Morris tried to evict folk singers from Washington Square Park, and the Church offered its Meeting Room for a series of "sing-ins" to protest that ruling - which was quickly overturned.   The 1990s found urban kids in the old Judson garden enjoying ice cream and jazz in the "Licks 'n' Licks" program on Sunday afternoons.

In the church's Sunday worship services, Judson Church members enjoy expertly-performed music, provided by the church’s music director – a position that, over the years, has employed  musicians with a variety of musical styles. When Al Carmines, a musical theatre composer and performer, was associate pastor in the 1970s, he also led the music, teaching the congregation to sing out full-voice on hymns.  From 1965-69, the music director was Edward Brewer, a harpsichordist and organist; he also presented several concert series of classical music and produced a Saturday midnight chamber music series. Paul Knopf, a jazz pianist still active in the Village, has led worship music on occasion, including performing his own compositions on the Psalms for several Thanksgiving services.  In the 1980s, music director Michael Kelly produced concerts by the church choir and guest instrumentalists from the Manhattan School of Music where he was on the piano faculty.  In the early 2000s, Chanelle Schaffer brought a jazz/show tunes sensibility to Judson worship. Current music director Michael Conley is also the conductor of two classical music vocal ensembles, the West Village Chorale and the Westchester Choral Arts Society, and is currently producing an ongoing series of concerts at the church under the title “Judson Arts.”