Anuradhapura became Sri Lanka's first capital in 380 BC under King Pandukabhaya, but it was under Devanampiya Tissa (r 307–267 BC) – during whose reign Buddhism reached Sri Lanka – that it first rose to great importance. Soon Anuradhapura became a great and glittering Buddhist complex, the importance of which was reinforced when the relic of Buddha's tooth was enshrined in the city in the 4th century AD.

In 204 BC the city was captured for the first time by the South Indian Chola dynasty – a fate that was to befall it repeatedly for more than 1000 years. It was almost a half-century until the Sinhalese hero Dutugemunu led an army from a refuge in the far south to recapture Anuradhapura. The ‘Dutu’ part of his name, incidentally, means ‘undutiful’ because his father, fearing for his son’s safety, forbade him to attempt to recapture Anuradhapura. Dutugemunu disobeyed him, and later sent his father a woman’s ornament to indicate what he thought of his courage.

Dutugemunu (r 161–137 BC) set in motion a vast building program that included some of the most impressive monuments in Anuradhapura today. Other important kings who followed him included Valagamba (r 103 BC and 89–76 BC), who lost his throne in another Indian invasion but later regained it, and Mahasena (r AD 276–303), the last ‘great’ king of Anuradhapura, who was the builder of the colossal Jetavanarama Dagoba. He also held the record for water-tank construction, building 16 of them in all, plus a major canal.

Anuradhapura was to survive until the early 11th century before finally being replaced as capital by Polonnaruwa. The Anuradhapura site was sacked by the Cholas in 1017 and never retained its earlier heights, though a handful of monks continued to live here for another 200 years.