It was here that King John I gathered the Council that decided on the conquest in 1415 of Ceuta, a Spanish enclave in North Africa, that marked the beginning of the outward-looking policies of Portugal.

In 1510, Torres Vedras received a municipal charter (Foral), and six years later King Manuel I, ordered reconstruction of the castle.

In 1589, during the Philippine dynasty (1581-1640), forces of António, Prior of Crato commanded by Sir Francis Drake disembarked in Peniche and briefly took the Castle of Torres Vedras.

Together with the Fort of São Vicente on a hill immediately to its north, the castle, with about 500 soldiers, guarded the main road between Coimbra and Lisbon.

During the so-called Little Civil War in 1846, it served as barracks for the troops of the Count of Bonfim and was bombarded by the forces of the Duke of Saldanha, which caused the almost total ruin of the Palace.