This study aims to fill a gap in legal and historical literature, approaching the unique ecclesiastical institutional phenomenon of the Ionian Church as a whole and abstractly, with a panoramic perspective and without focusing on individual islands or specific stages of its historical course. It thoroughly examines, from the perspective of a legal scholar of Ecclesiastical Law, the genesis, gradual formation, evolution, and functioning of the institutions and organs of the Ionian Church, as well as the criticism it received from contemporary political and ecclesiastical actors through legal or canonical arguments, as a living organism at that time. Furthermore, given the survival of individual institutions and regulations of Ionian Church Law in the years following the Union, it contributes to contemporary judicial practice by appropriately utilizing and supplementing unknown or repealed legislative provisions of that era.