The Vestry supports the Dean and other clergy in making the Cathedral a welcoming spiritual home for parishioners and visitors.  Its special responsibilities include oversight of parish finances, care of the parish buildings, and choosing of individuals to fill various positions of parish leadership and representation. The Vestry of the American Cathedral is composed of 15 members elected by the congregation at its Annual Meeting. A vestry member is elected for a three-year term, with the possibility of being elected for a second three-year term. After two terms, a vestry member must rotate off for three years before serving again.  Terms are staggered so that one-third of the vestry is elected each year.

Vestry officers are Senior Warden (appointed by the Dean), Junior Warden, Treasurer, and Clerk, all elected by the vestry.

The vestry meets monthly from September through June and has a weekend retreat each year.