Following the establishment of Constantinople (the ancient city of Byzantium) as the state capital of the Roman Empire in the early part of the fourth century, a series of significant ecclesiastical events saw the status of the Bishop of New Rome (as Constantinople was then called) elevated to its current position and privilege. The Church of Constantinople is traditionally regarded as being founded by St. Andrew, the "first-called" of the Apostles. The 3rd canon of the Second Ecumenical Council held in Constantinople (381) conferred upon the bishop of this city second rank after the Bishop of Rome. Less than a century later, the 28th canon of the Fourth Ecumenical Council held in Chalcedon (451) offered Constantinople equal ranking to Rome and special responsibilities throughout the rest of the world and expanding its jurisdiction to territories hitherto unclaimed.

The Ecumenical Patriarchate holds an honorary primacy among the autocephalous, or ecclesiastically independent, Churches. It enjoys the privilege of serving as "first among equals." It is also known as the "Roman" Patriarchate (hence the Turkish phrase: Rum Patrikhanesi), recalling its historical source as the Church of New Rome, the new capital of the Roman Empire, transferred in 330 from Old Rome to Byzantium by Constantine the Great. The first bishop of the city of Byzantium was St. Stachys (38–54), a disciple of the Apostle Andrew. In 330, Byzantium was renamed Constantinople and New Rome, while its bishopric was elevated to an archbishopric. The Metropolitan of Heraclea, to whom Byzantium was formerly subject, now came under the jurisdiction of Constantinople and enjoyed the privileges of the latter's most senior see.

As a title, the phrase "Ecumenical Patriarchate" dates from the sixth century and belongs exclusively to the Archbishop of Constantinople. The Great Schism of 1054—in fact the culmination of a gradual estrangement over many centuries—resulted in formal separation between the Churches of the East and the West, granting Constantinople sole authority and jurisdiction over the Orthodox Churches throughout the world.

After the capture of Constantinople by the Latins during the Fourth Crusade (1204), the Ecumenical Patriarchate was transferred to Nicaea (1206), but Emperor Michael VIII Palaeologos restored it to Constantinople when he recaptured the city in 1261. When Constantinople became the capital of the Ottoman Empire in 1453, the Ecumenical Patriarch (at the time, Gennadius II) was recognized as Ethnarch of the Orthodox peoples, with increased authority over the Eastern Patriarchates and the Balkan Churches, as well as farther afield.

From that time, the Ecumenical Patriarchate became a symbol of unity, rendering service and solidarity to the Eastern Churches. In difficult periods, the Ecumenical Patriarchate was consulted for the resolution of problems. Frequently, patriarchs of other Churches would reside in Constantinople, which was the venue for meetings of the Holy Synod that was chaired by the Ecumenical Patriarch.

The Ecumenical Patriarchate also sponsored missionary growth through the centuries, the most notable of which was the conversion of the Kievan Rus in the tenth century and the most recent of which was the missionary work in Southeast Asia in the last century. This pastoral role and responsibility has earned the characterization of the Ecumenical Patriarchate as "the golden beacon of Orthodoxy, preserving the unwaning brilliance of Christianity."

Currently, the Ecumenical Patriarchate is actively engaged in diverse ecclesiastical activities and ministries. It has historically proved to be a dynamic leader in the ecumenical movement, fully participating in the World Council of Churches from its inception, as well as in local ecumenical bodies instituting and chairing bilateral theological dialogues with non-Orthodox Christians but also with other monotheistic faiths.