Cirrha began as the harbour of the older inland city of Crissa, following a pattern common across the ancient Greek world: the original settlement sits on a defensible height, and when times grow more settled, a second town grows up at the coast to handle trade. Cirrha occupied the mouth of the river Pleistus, at the foot of Mount Cirphis, on the small coastal plain that opens onto the Gulf. From there it controlled the sea approach to Delphi. Pilgrims bound for the oracle — and they came from across the Greek world — had to disembark at Cirrha and make the journey up through the plain and into the mountains beyond. The Cirrhaeans did not let that opportunity pass quietly. They levied heavy tolls on the pilgrims and were accused, in the language of the era, of mistreating Phocian women returning from the sanctuary. Whether the charges were exaggerated for political convenience is impossible to say now; what is clear is that they gave the Amphictyonic League — the inter-state council that governed Delphi's affairs — the justification it needed.

Around 595 BCE, the Amphictyons declared what history calls the First Sacred War against Cirrha. The conflict ground on for roughly a decade before the city was finally taken, perhaps around 585 BCE. The outcome was categorical. Cirrha was razed to the ground. Its harbour plain was consecrated to Apollo and placed under a formal religious curse: the land could not be tilled, no one could dwell on it, and livestock could not graze it. The spoils of the city funded the Pythian Games, which the Amphictyons instituted — or reorganised — in the aftermath of the war. The Hippodrome that served those games stood in the Cirrhaean plain by the sea. Pindar, writing in the fifth century BCE, still mentioned a Stadium there as well, though it was later moved up the mountain to Delphi itself. The plain remained conspicuously bare for generations, a visible monument to the consequences of insulting Apollo's pilgrims.

Two centuries after the destruction, the curse was broken — or tested — by the people of Amphissa, who cultivated the sacred plain and began to rebuild the ruined town. This provoked the Fourth Sacred War and ultimately drew in Philip II of Macedon, to whom the Amphictyons entrusted the campaign. Philip took Amphissa in 338 BCE, the same year his victory at the Battle of Chaeronea established Macedonian dominance over the Greek world. The irony was perfect: a quarrel over the ruins of a destroyed port helped give one man control of Greece. Cirrha was rebuilt eventually — the historian Polybius mentions it, and by the second century CE, when Pausanias travelled through, it held a temple shared by Apollo, Artemis, and Leto, with statues he described as Attic work. The city had come back, quieter and smaller, still serving as the port of Delphi.

The site of ancient Cirrha is identified at a hill called Magoula Xeropigadas, near the modern village of Kirra — a name that preserves the ancient sound across two and a half millennia. Kirra is part of the municipal unit of Itea, on the northern shore of the Gulf of Corinth. By the mid-nineteenth century, surveyors could still trace the remains of walls enclosing a roughly quadrangular space about 1.6 kilometres in circuit, with foundations of buildings scattered inside and outside that perimeter. The Cirrhaean plain — the small coastal strip between the sea and the twin projecting rocks that divide it from the larger, more fertile Crissaean plain above — is still distinct, still framed by Parnassus to the north and Mount Cirphis to the east. The boundaries of the land once dedicated to Apollo were inscribed on one of the walls of the Delphic temple. The inscription is gone, but the plain is still, for the most part, open.