John Zizioulas’ theology finds its genesis in the profound recognition that the entirety of the Church’s reality and life emanates from the mystery of the Eucharist, celebrated by the ecclesial community gathered around its bishop.

For Zizioulas, theology commences with the encounter of God in Christ, actualized by the Holy Spirit, within the Eucharistic milieu. Since the era of early Christians, the term "Church" was virtually synonymous with the eucharistic assembly. If the Church is indeed the Body of Christ, then the Church is inherently the Eucharist, for it is here that the congregation of the faithful is constituted into the Body of Christ. To Zizioulas, the Pauline notion of the “Body of Christ” is not figurative; the Eucharist is, quite literally, the manifestation of the resurrected Body of Christ. This reality transpires due to the presence of the Holy Spirit, who shapes the faithful into the Body of Christ, thereby not merely inspiring or empowering individual Christians but culminating the work of Christ by making tangible the uncreated-created communion achieved in the person of the resurrected Christ.

Zizioulas’ extensive inquiry aims to scripturally ground several systematic positions, particularly the doctrine of the Holy Eucharist. Notably, he elucidates the six facets of this theology that had grown somewhat faint within Western theology and, consequently, in contemporary Orthodox Dogmatics. These facets encompass: a) the perception of the Eucharist as a gathering and as a community, b) the spiritual character of the Eucharist, c) the eschatological nature of the Eucharist, d) the cosmic or cosmological dimensions of the Eucharist, and e) the ecclesiological significance of the Eucharist.

Zizioulas has significantly contributed to eucharistic ecclesiology by advancing N. Afanasyev's Eucharistic theology and expanding on the ideas of H. de Lubac, with whom he shares fundamental insights.

Already within his doctoral dissertation, John Zizioulas contends that the celebration of the Eucharist (and, correspondingly, the very establishment of the Church) is intrinsically and indissolubly tied to the unique role of the presiding figure of the Eucharist, namely, the bishop. Zizioulas diverges from theologians such as Afanasyev and Meyendorff, whom he construes as asserting that the Church attains its fullness wherever the Eucharist is conducted, effectively rendering the parish, as a eucharistic community, the foundation of the catholic Church. He firmly posits that “the Church constitutes the Eucharist while being constituted by it.” He aims to amplify Afanasiev’s perspectives, particularly by underscoring the necessity of celebrating the Eucharist in communion with the local Church, presided over by the bishop, and in communion with the universal Church. In Zizioulas’ perspective, the catholic Church is fully actualized solely in the eucharistic gathering led by the bishop (hence, the existence of parishes represents a concession to presbyters from the bishop). However, this eucharistic assembly under the bishop must be celebrated in canonical communion with all other eucharistic assemblies. These matters persist as a subject of spirited debate and exploration.

Beginning with the New Testament accounts pertaining to the Eucharist, Zizioulas progresses to the established order of the Eucharist, rooted in the Last Supper within the apostolic Church. Despite the scarcity of information concerning the Eucharist, he reveals a strong link between the Eucharist and the Mystery of the Church. The Eucharist does not derive from family life events (such as the Paschal meal) but rather from occurrences within the “friends of the lamb,” signifying a liberated communion resulting from the Eschaton penetrating history. The synaxis participating in the Last Supper unveils the eschatological nature of the Church and, by the action of the Holy Spirit, portrays Christ as an existential reality intertwined with the Church's historical dimension. The Holy Spirit “reminds” the Church of Christ, reenacting His presence within its life. The Eucharist, as a manifestation of a “catholic Church,” transcends societal divisions and those arising from age, gender, race, and the like. All occurrences within the Eucharist do not form a parallel reality to the heavens; they are one and the same. The divine life imparted through the Eucharist shapes not only what God accomplishes and conveys in Christ but also God Himself. Consequently, Christ desires that the Eucharist be not a commemoration of “His acts and His teachings” but a rememberance of “Him.”

The relationship “Eucharist-world” carries a more favorable tone, explored through the lens of the New Testament. The Eucharist embodies an envisioned eschatological unity of the people of God, with the synaxis structure mirroring the very essence of the Church itself. The person presiding over this synaxis stands in the place of the One through whom “many” have become one Body. Eucharistic communion simultaneously constitutes both communio in sacris and communio sanctorum (communion through the holy and the communion of the saints).

Drawing from Nicholas Cabasilas’s assertion that the Church is “indicated” in the Eucharist, there is a heightened emphasis on the Church becoming its true self when it partakes in the Eucharist. It is on the Eucharist that all the other parameters of the community—structure, administration, morality, sacraments—depend for their meaning and the form they take. The Eucharist is not just a spiritual remedy fortifying believers for their spiritual struggles; it constitutes the event from which every Church member derives their identity. It offers a preview of the Kingdom that will be fully realized in the future, encompassing its cosmic dimensions.

Metropolitan John extrapolates from this liturgical worldview and ethos an inspiration for a Eucharistic ecology—an approach to serving and managing the material world and environment inspired by liturgical ethos. The Church experiences, in the Eucharist, not only the “actualization of Christ’s sacrifice on the Cross” but also the eschatological Kingdom and the transformation of the world.