Kudiramalai is the northernmost point of Puttalam District and was a southern port of Mannar during the classical period, serving the northern kingdoms of the Jaffna Peninsula and Vanni country as one of their southernmost border towns.

Rulers included Alli Raani, Korran, his father (Pittan) and contemporaries, Athiyamān Nedumān Añci and his son Kumanan.

Kudiramalai shares the legends of the Tamil queen Alli Raani with Mannar; during her rule, major changes to the western coastline occurred.

French biblical scholar Samuel Bochart first suggested Tamilakam, whose people were known for their gold, pearl, ivory and peacock trade, for the ports of Ophir and Tarshish during King Solomon's reign.

Kudiramalai shared a similar Tamil name with the northern Sri Lankan port of Kandarodai, known as Kadiramalai, on the Jaffna Peninsula.

Nearby Puttalam was the medieval Jaffna kingdom's second capital during the pearling season, and increased fishing activity was noted along the banks between Kudiramalai and Mannar.

Mukkuvar Tamils began migrating from Kilakarai in mainland Tamilakkam to Kudiramalai and other Malabar cities (such as Puttalam and Jaffna) of the northern kingdom during the eighth century.