Ancient tradition held that Cyzicus was founded by Pelasgians from Thessaly, arriving at the time of the legendary Argonauts — which places its mythological founding in the age of heroes. Historical colonization came later, with settlers from Miletus arriving allegedly around 756 BC. But the city's real rise came during the Peloponnesian War (431–404 BC), when the conflict between Athens and Sparta centered on the sea lanes between Greece and the Black Sea. Cyzicus sat at the junction of those lanes, on the peninsula then known as Arctonnesus — the Bear Peninsula — which was either still an island or newly connected to the mainland.

Commercial power followed geographic advantage. The gold staters of Cyzicus became a standard currency across the ancient Greek world, displacing rivals until Philip of Macedon's coins superseded them. The distinctive Cyzicene coin, the cyzicenus, was worth 28 drachmae — a meaningful denomination in a world that ran on silver. The philosopher Eudoxus of Cnidus established a school at Cyzicus in the 4th century BC, visited Plato in Athens with his pupils, and died around 350 BC; his presence suggests that by then the city was attracting intellectual as well as commercial life.

During the Peloponnesian War, Cyzicus changed hands between Athens and Sparta repeatedly. The Athenian general Alcibiades defeated the Spartan fleet in a decisive engagement off the city in 410 BC, retaking it — the Spartan dispatch that survived reads simply: "The ships are gone. Mindarus is dead. The men are starving. We know not what to do." At the peace of Antalcidas in 387 BC, the city was handed to Persia along with the other Greek cities of Asia Minor. Alexander the Great captured it from the Persians in 334 BC.

Through the Hellenistic period, Cyzicus was closely tied to the Attalid kings of Pergamon. When the Attalid dynasty ended with Rome as its heir, Cyzicus became a Roman-allied city of considerable importance. Under the emperor Tiberius it was formally incorporated into the Roman Empire, serving as the capital of Mysia and later of the province of Hellespontus. Roman favor brought investment: the great amphitheater, with a diameter of nearly 500 feet and construction spanning the 1st through 3rd centuries AD, was one of the largest in the Roman world.

The Temple of Hadrian at Cyzicus was built in the 2nd century AD to honor the emperor Hadrian, who visited the city. Its scale was extraordinary. The columns, at 21.35 meters, exceeded in height those of every other known temple in the Greco-Roman world — the columns at Baalbek in Lebanon, often cited as the tallest, stand 19.35 meters. Some ancient writers ranked the Cyzicus temple among the Seven Wonders of the ancient world, though it does not appear on the canonical lists.

Thirty-one of its columns were still standing in 1444. After that date, the record goes silent — the columns were removed systematically, first by Byzantine quarriers working for Justinian's construction of Hagia Sophia, and later by Ottoman builders. Nothing above ground remains. The substructures — the massive foundations — are still partly visible beneath the marshland of Bal-Kız, along with sections of the Roman city walls dating from the 4th century and the remnants of a Roman aqueduct. The amphitheater site, intersected by a stream, can be located north of the main city area. These fragments, spread across a large area, give some sense of how extensive the ancient city was.

Cyzicus was an early and important center of Christianity. As capital of the Roman province of Hellespontus, it became an ecclesiastical metropolitan see, with twelve suffragan bishoprics by the 7th century. The city produced or hosted notable figures: the theologian Eunomius; bishops Proclus and Germanus, both later Patriarchs of Constantinople; the martyr Saint Emilian in the 8th century; and Saint Tryphaena of Cyzicus, patron of the city. Before Christianity, the city had hosted a women's cult of Artemis called the Dolon.

Earthquakes proved more destructive than any army. A series of tremors beginning in 443 AD progressively damaged the city; the last significant earthquake came in 1063. The population transferred to nearby Artake before the 13th century. Arab forces under Muawiyah I had seized the city temporarily in 675 AD. The Crusaders occupied the peninsula in the 13th century. Through all of this the metropolitan see persisted, its bishops serving a diminished city, until the 1923 Convention Concerning the Exchange of Greek and Turkish Populations ended the Greek Orthodox community there entirely. The last bishop died in 1932.

The site of Cyzicus today is quiet in the way that places become quiet when they have absorbed too much history to speak about it simply. Bal-Kız — the local name for the ruins area — lies off the road between Erdek and Bandırma, its fields grown over the foundations of a city that once struck gold coins that circulated from the Black Sea to the Aegean. The Ministry of Culture protects it; archaeologists have worked portions of it; but large-scale excavation has not happened. Most of what Cyzicus was still lies underground.

What can be seen above ground — traces of walls, sunken foundations, scattered stone — requires imagination to read. But the scale is undeniable. The distance between the amphitheater site to the north and the temple foundations to the south is substantial, reminding any visitor that this was not a minor town but a metropolis: capital of a province, seat of bishops, home of philosophers, mint of coins that half the ancient world used. Its silence now is proportional to the noise it once made.