The Middle Ages is rightly considered the golden age of the prominent castle-town of Methoni. Its medieval glory is depicted in the strong walls, a work of the Venetians, who expelled the Frankish garrison of Godfrey de Villehardouin in 1206 and captured it in 1209 with the signing of the Treaty of Sapienza.

When the Venetians took over Crete, Methoni became a bastion of their colony in the competition with the Genoese. The area of the castle evolved into a station towards the shores of Asia and the Holy Lands. Western chroniclers refer to the Peloponnese as "the Isle of Methoni" (L'île de Modon).

The significance of the castle is highlighted by the proclamation of Doge A. Barbarigo in 1500 (after its capture by the Turks) to the Pope, the King of Spain, and other princes: "we have lost the exquisite stronghold of all the ships which traveled to the East."

After the naval battle of Navarino, the liberating forces of General Maison built the new Methoni outside the walls. What remains standing today inside the castle are ruins of Turkish hammams and a minaret, underground cisterns, a powder magazine, and the church of the Transfiguration of Christ.