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The Anuradhapura Kingdom, named for its capital city, was the first established kingdom in ancient Sri Lanka and Sinhalese people. Founded by King Pandukabhaya in 377 BC, the kingdom's authority extended throughout the country, although several independent areas emerged from time to time, which grew more numerous towards the end of the kingdom. In 543 BC, prince Vijaya (543–505 BC) arrived in Sri Lanka, having been banished from his homeland in India. He eventually brought the island under his control and established himself as king. After this, his retinue established villages and colonies throughout the country. One of these was established by Anuradha, a minister of King Vijaya, on the banks of a stream called Kolon and was named Anuradhagama.

In 377 BC, King Pandukabhaya (437–367 BC) made it his capital and developed it into a prosperous city. Anuradhapura was the capital of all the monarchs who ruled the country during in the Anuradhapura Kingdom, with the exception of Kashyapa I (473–491), who chose Sigiriya to be his capital. The city is also marked on Ptolemy's world map. The king of Anuradhapura was seen as the supreme ruler of the country throughout the Anuradhapura period. Buddhism played a strong role in the Anuradhapura period, influencing its culture, laws, and methods of governance. Society and culture were revolutionized when the faith was introduced during the reign of King Devanampiya Tissa; this cultural change was further strengthened by the arrival of the Tooth Relic of the Buddha in Sri Lanka and the patronage extended by her rulers.

Invasions from South India were a constant threat throughout the Anuradhapura period. Rulers such as Dutthagamani, Valagamba, and Dhatusena are noted for defeating the South Indians and regaining control of the kingdom. Other rulers who are notable for military achievements include Gajabahu I, who launched an invasion against the invaders, and Sena II, who sent his armies to assist a Pandyan prince. Under Dutthagamani (161–137 BC), the whole country was unified under the Anuradhapura Kingdom. He defeated 32 rulers in different parts of the country before he killed Elara, the South Indian ruler who was occupying Anuradhapura, and ascended to the throne. Because the kingdom was largely based on agriculture, the construction of irrigation works was a major achievement of the Anuradhapura Kingdom, ensuring water supply in the dry zone and helping the country grow mostly self-sufficient. Several kings, most notably Vasabha and Mahasena, built large reservoirs and canals, which created a vast and complex irrigation network in the Rajarata area throughout the Anuradhapura period. Saddha Tissa (137–119 BC), Mahaculi Mahatissa (77–63 BC), Vasabha (67–111), Gajabahu I (114–136), Dhatusena (455–473), Aggabodhi I (571–604) and Aggabodhi II (604–614) were among the rulers who held sway over the entire country after Dutthagamani and Valagamba.

The bhikkhuni Sanghamitta (daughter of King Ashoka) of arrived from India in order to establish the Bhikkhuni sasana (order of nuns) in the country. She brought along with her a sapling from the Sri Maha Bo