At the end of the same century, amid political turmoil and conflict, Parga’s inhabitants, following the example of their Corfiot neighbours, sought protection from the Republic of Venice. In 1401, they signed a treaty that made Parga a Venetian possession. The Venetians granted them privileges, transforming Parga into an important trading post and base for the Venetians, serving as the “eye and ear” of Corfu on the Epirus coast for the next four centuries.

The Ottomans occupied Parga in 1452, and two years later, in 1454, it returned to the Venetians, thanks to the mobilisation of the Pargians and Corfiots. At the same time, only small-scale fortification works were carried out due to lack of resources, even though the city feared an imminent attack by the Ottomans, who had already burned the castle twice by the early 16th century. In 1537, the Ottoman fleet under Hayreddin Barbarossa Parga destroyed Parga, but the Venetians reconstructed it in 1567. In 1571, the Ottoman fleet destroyed it again during raids on Venetian possessions in the Ionian Sea shortly before its defeat in the naval Battle of Lepanto the same year. The Venetians quickly restored and expanded the castle and, in the 17th century, Parga entered a period of prosperity, with the settlement growing beyond its walls.

After 1797 and the dissolution of the Republic of Venice, Parga went through a period of instability and insecurity. In 1797, Parga passed to the French, then in 1800 formally to the Ottomans, but under Russian protection. In 1807, it returned to the French, and finally, in 1814, it passed to the British. These successive changes of rulers and protectors prevented Parga from falling into the hands of its greatest enemy, Ali Pasha of Ioannina, who had already secured all the other Venetian bases on the Ionian coast by 1817. However, in that year, the British governor of the Ionian Islands, Thomas Maitland, signed a treaty ceding control of Parga to Ali Pasha in exchange for a monetary settlement. Its residents were given the option to stay or leave and to be compensated for their properties. Shortly before the castle was handed over to Ali Pasha in 1819, most inhabitants left their homeland and took refuge in the Ionian Islands, mainly Corfu. The castle fell into disrepair and was gradually abandoned in the second half of the 19th century.