Initially mentioned in the Ṛgveda for their sheep's wool, the Gandhārīs were part of the distant tribes known to the Vedic people, alongside the Mūjavants, Āṅgeyas, and Māgadhīs. During the Vedic period, the Gāndhārī king Nagnajit and his successor were noted for their Brahmanic consecration, though their religious practices leaned towards non-Brahmanical traditions, with Nagnajit reportedly adopting Jainism or achieving a form of Buddhist enlightenment.

By the later Vedic era, Gandhāra, with its capital at Takṣaśila, emerged as a significant center of education and philosophy, attracting students from across the region, including the renowned Uddālaka Āruṇi. By the 6th century BCE, Gandhāra had grown into a formidable imperial power, exerting suzerainty over neighboring states in the Punjab region and engaging in expansionist conflicts, yet also maintaining diplomatic ties, as seen with King Pukkusāti's relations with Bimbisāra of Magadha.

Gandhāra was recognized as one of the sixteen Mahājanapadas, indicative of its major role in the Iron Age of South Asia. However, its prominence attracted the attention of the Persian Achaemenid Empire, leading to its conquest by Cyrus the Great in the late 6th century BCE. While some scholars suggest Pukkusāti might have resisted Persian expansion, ultimately, Gandhāra was annexed into the Achaemenid Empire, a fact confirmed by its inclusion in Darius's Behistun Inscription. The extent of Persian control and Pukkusāti's fate post-conquest are subjects of historical speculation, with some sources suggesting he renounced his throne to become a monk. The Achaemenid conquest marked a significant shift in Gandhāra's history, leading to a realignment of power in the region.