The ancient Athenian Supreme Court once occupied this rocky hill. Judging cases from murder and arson to sacrilege, the court even made decisions on new religious ideas. It is believed that this location got its name from one of two sources, the first being the murder trial of the god, Ares who was tried for the murder of Allerothios, son of Poseidon.

The second theory is that its name came from the temple of the Areian Erinyes, the sinister deities of punishment, scruples and revenge.

From the Mycenaean to the Geometrical era (1600-700 BC), the northern slope of the hill was used as a cemetery. During the late Roman era four mansions were built on the Areopagus that were replaced in the 15th and 16th centuries by a church honouring Saint Dionysius Aeropagite, the first Christian bishop of Athens.

All later buildings from the Classical era were removed during the Ottoman rule.