South of the Bouleuterion is the Prytaneion. Between them, remains are visible of the West Gate of the old 4th century BC precinct, through which the Sacred Way passed leaded to the oracular Oak-tree. For the construction of the two buildings, the Hiera Oikia and the Prytaneion, it was necessary to move the west side of the precinct further west and to join in with the House of the Priests.

The Prytaneion comprises the original nucleus, 31.50 m wide, dating to the beginning o the 3rd century BC and the extension to the north side made at the end of the 3rd century BC. This consists of three rooms with nine couches each and with service areas, where the archontes (government officials) dined, and on the east side, of a large extended colonnade that extended nearly as far as the south-west main gate of the west perimeter wall.

These additions were considered necessary when the Epirote Alliance was succeeded by the Epirote League, which was joined by all the Greek Epirote tribes from southern Albania to the Ambracian Gulf.

The Prytaneion, in whose sacred hearth the eternal fire burned, was where the prytaneis (magistrates) and distinguished persons dined and the resolutions of the Boule and the archontes were kept. It was, in a way, the home of the city-state or city-tribe. The excavations, which are continuing, brought to light a peristyle court with 4 x 4 Doric columns on the east side, where the entrance was.

After the Roman destruction in 167 BC, the Prytaneion was roughly repaired in the 1st century BC, but the north wing and its rooms with nine couches each and the east colonnade remained buried beneath the rubble. The Doric peristyle belonging to the beginning of the 3rd century BC was replaced by a larger one (4 x 7 columns) carelessly constructed of various materials. The bases of the peristyle, which was now built on a larger scale, consisted of slabs taken from the destroyed pedestrals that had been on the east facade of the Ionic Stoa. One of these bases preserves part of a decree by the League (of Epirotes), which tells us that the League, after an oracle, honoured a certain person with a bronze statue signed by a hitherto unknown sculptor, Melissos, son of Epikrates, from Corcyra.