The narrative begins with King Çūdraka of Ujjayinī receiving a learned parrot named Vaiçampāyana, brought by a mysterious Caṇḍāla maiden who declares herself to be Lakshmī. The parrot recounts its origin in the Vindhyā Forest, where it was born to aged parents who died of grief. Rescued and brought to the hermitage of the sage Jābāli, the parrot hears the epic history of its former life as Vaiçampāyana, the son of the minister Çukanāsa, and his companion Candrāpīḍa, the prince of Ujjayinī. Candrāpīḍa embarks on a world conquest, reaching the Acchoda Lake where he meets the ascetic Mahāçvetā.
She narrates her tragic love for the young Brahman Puṇḍarīka, who died of lovesickness, and her friend Kādambarī, who vowed never to marry while Mahāçvetā remained in sorrow. Candrāpīḍa falls in love with Kādambarī at first sight before urgent affairs call him back to Ujjayinī. Meanwhile, Vaiçampāyana remains at the lake and falls into a strange trance.
When Candrāpīḍa returns to find him, he learns that Mahāçvetā, in her despair, laid a curse that turned the offending Vaiçampāyana into a parrot. Overcome by grief at his friend's fate, Candrāpīḍa dies on the spot. Kādambarī arrives and nearly takes her own life, but a voice from the sky promises eventual reunion with their lovers. The narrative circles back to King Çūdraka, who suddenly remembers his past life as Candrāpīḍa and dies of longing. A touch from Kādambarī restores him, breaking the ancient curse. All the principal characters, having suffered through multiple earthly births, are finally reunited with their beloved companions in everlasting happiness.