A lord of the Teleri in Middle-earth, Círdan was persuaded to remain in Beleriand with some of his people by Ossë when the other Teleri were taken into the West by Ulmo. He remained Lord of the Falas during much of the First Age, but removed to the Isle of Balar after the Nirnaeth Arnoediad. At the end of the First Age, with the destruction of Beleriand, he moved eastwards and founded Mithlond, the Grey Havens, on the Gulf of Lhûn.

Lindon remained his home throughout the Second and Third Ages. Throughout the Second Age, that land was under the direct rule of High King Gil-galad. At the time of the fall of Eregion, Celebrimbor sent two of the Three Rings north to the High King, and Gil-galad in turn passed one of these to Círdan; Narya, the Ring of Fire. At the end of the Second Age, Gil-galad fell in the War of the Last Alliance, leaving Lindon without a ruler. His natural heir would have been Elrond, but Elrond had long since removed to Imladris, and so Círdan took on the leadership of the Elves west of the Blue Mountains.

Círdan continued to maintain the havens at Mithlond throughout the Third Age and into the Fourth. When the Wizards arrived in Middle-earth, he perceived that Gandalf was the wisest of them, and gave him the Red Ring to bear in secret. He took an active part in the events of the Third Age, too; it was his mariners, for example, who sought to rescue Arvedui the last King of Arthedain. He was still the Master of the Grey Havens at the end of the Age, when he saw the Ring-bearers' White Ship, which he had held in preparation over the long years, pass into the West.