Ancient Afghan: Achaemenid invasion and Zoroastrianism (550 BC–331 BC)

The city of Bactria (which later became Balkh), is believed to have been the home of Zarathustra, who founded the Zoroastrian religion. The Avesta refers to eastern Bactria as being the home of the Zoroastrian faith.

[Arachosia, Aria and Bactria were the more eastern ancient satraps of the Achaemenid Empire that made up most of what is now Afghanistan during 500 B.C. The inhabitants of Arachosia were known as Pactyans, possibly today's Pakhtuns or Pashtuns.]

Regardless of the debate as to where Zoroaster was from, Zoroastrianism spread to become one of the world's most influential religions and became the main faith of the old Aryan people for centuries. It also remained the official religion of Persia until the defeat of the Sassanian ruler Yazdegerd III—over a thousand years after its founding—by Muslim Arabs.

In what is today southern Iran, the Persians emerged to challenge Median supremacy on the Iranian plateau. By 550 BC, the Persians had replaced Median rule with their own dominion and even began to expand past previous Median imperial borders.

Both Gandhara and Kamboja Mahajanapadas of the Buddhist texts soon fell prey to the Achaemenian Dynasty during the reign of Achaemenid, Cyrus the Great (558–530 BC), or in the first year of Darius I, marking the region or of the easternmost provinces of the empire, located partly in nowadays Afghanistan.

According to Pliny's evidence, Cyrus the Great (Cyrus II) had destroyed Kapisa in Capiscene which was a Kamboja city. The former region of Gandhara and Kamboja (upper Indus) had constituted the seventh satrapy of the Achaemenid Empire and annually contributed 170 talents of gold dust as a tribute to the Achaemenids. Bactria had a special position in old Afghanistan, being the capital of a vice-kingdom.

By the 4th century BC, Persian control of outlying areas and the internal cohesion of the empire had become somewhat tenuous. Although distant provinces like Bactriana had often been restless under Achaemenid rule, Bactrian troops nevertheless fought in the decisive Battle of Gaugamela in 330 BC against the advancing armies of Alexander the Great.

The Achaemenids were decisively defeated by Alexander and retreated from his advancing army of Greco-Macedonians and their allies. Darius III, the last Achaemenid ruler, tried to flee to Bactria but was assassinated by a subordinate lord, the Bactrian-born Bessus, who proclaimed himself the new ruler of Persia as Artaxerxes (V).

Bessus was unable to mount a successful resistance to the growing military might of Alexander's army so he fled to his native Bactria, where he attempted to rally local tribes to his side but was instead turned over to Alexander who proceeded to have him tortured and executed for having committed regicide.