Together with the Castello di Santa Margherita Ligure to the west and the Castello di Rapallo to the east, Castello di Punta Pagana formed part of the Genoese coastal defence system for the protection of villages on the western Tigullio gulf.
Construction of the fort began in April 1625 by the Republic of Genoa. Its construction became necessary due to the open hostilities between Genoa and Charles Emmanuel I, Duke of Savoy, which raised fears of a Piedmontese land or sea attack.
The fort cost over 50,000 lire, and construction work progressed rapidly thanks to new taxes that allowed for the purchase of the material and paying workers' salaries. Construction was well underway by December 1625, and the moat and drawbridge were ready by 1627. The fort was fully completed and commissioned by the Republic of Genoa on 28 July 1631. It was armed with enough weapons, ammunition and gunpowder for a sudden attack.
Fortunately for the inhabitants of the nearby village of San Michele di Pagana, the area was never attacked by pirates or enemy soldiers and the fort never saw use. In 1644, the Genoese senate ordered the castellan to abandon the fort and send all military equipment inside on a galley to Genoa.
The castle was subsequently garrisoned by local soldiers, and it became the headquarters of the Commissariato di Sanità di Rapallo (Health Commissariat of Rapallo). The Bombardment of Genoa by the French fleet in 1684 caused fears of another attack, so the fort was rearmed. However, no attacks occurred, and the fort was finally abandoned in 1705. It later became private property, forming part of the grounds of the nearby Villa Pagana.
The fort has belonged to the Sovereign Military Order of Malta since 1959, when the last owner of the villa passed on the entire property to the Order.
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