In 377 BC, King Pandukabhaya (437–367 BC) made it his capital and developed it into a prosperous city. Anuradhapura (Anurapura) was named after the minister who first established the village and after a grandfather of Pandukabhaya who lived there. The name was also derived from the city's establishment on the auspicious asterism called Anura. 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.
Another notable king of the Anuradhapura Kingdom is Valagamba (103, 89–77 BC), also known as Vatthagamani Abhaya, who was overthrown by five invaders from South India. He regained his throne after defeating these invaders one by one and unified the country again under his rule. 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. Rulers from Kutakanna Tissa (44–22 BC) to Amandagamani (29–19 BC) also managed to keep the whole country under the rule of the Anuradhapura Kingdom. Other rulers could not maintain their rule over the whole island, and independent regions often existed in Ruhuna and Malayarata (hill country) for limited periods. During the final years of the Anuradhapura Kingdom, rebellions sprang up and the authority of the kings gradually declined. By the time of Mahinda V (982–1017), the last king of the Anuradhapura Kingdom, the rule of the king had become so weak that he could not even properly organize the collection of taxes.
During the times of Vasabha, Mahasena (274–301) and Dhatusena, the construction of large irrigation tanks and canals was given priority. Vasabha constructed 11 tanks and 12 canals, Mahasen constructed 16 tanks and a large canal, and Dhatusena built 18 tanks. Most of the other kings have also built irrigation tanks throughout Rajarata, the area around Anuradhapura. By the end of the Anuradhapura Kingdom, a large and intricate irrigation network was available throughout Rajarata to support the agriculture of the country.
Soon afterwards, the bhikkhuni Sanghamitta 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 Bodhi, the tree under which the Buddha attained enlightenment, which was then planted in Anuradhapura. Devanampiya Tissa bestowed on his kingdom the newly planted Jaya Sri Maha Bodhi. Thus this is the establishment of Buddhism in Sri Lanka
The country was invaded again in 103 BC by five Dravidian chiefs, Pulahatta, Bahiya, Panya Mara, Pilaya Mara and Dathika, who ruled until 89 BC when they were defeated by Valagamba. Another invasion occurred in 433, and the country fell under the control of six rulers from South India. These were Pandu, Parinda, Khudda Parinda, Tiritara, Dathiya and Pithiya, who were defeated by Dhathusena who regained power in 459. More invasions and raids from South India occurred during the reigns of Sena I (833–853) and Udaya III (935–938). The final invasion during the Anuradhapura Kingdom, which ended the kingdom and left the country under the rule of the Cholas, took place during the reign of Mahinda V.
However, none of these invaders could extend their rule to Ruhuna, the southern part of the country, and Sri Lankan rulers and their heirs always organized their armies from this area and managed to regain their throne. Throughout the history of Sri Lanka, Ruhuna served as a base for resistance movements.