Disciples have a three-level polity: local congregations are the primary expression of the church; regional churches (previously called regions or state societies) provide coordination and support; and the General Assembly of the Christian Church (Disciples of Christ) is the highest deliberative body, meeting biennially. Theologically, each congregation is an expression of the whole church, not a subdivision of a hierarchical institution.

The 1968 Restructure transformed what had been a loosely federated fellowship into a more formally organized denomination with a written constitution (the Design). This created tension with some congregations that valued radical independence, contributing to the formation of the more conservative Independent Christian Churches as a separate fellowship. The Disciples polity attempts to balance congregational freedom with covenant relationships.