In the First Age, Círdan ruled of the Falathrim of the havens of Eglarest and Brithombar, although he seemed to had accepted Thingol's overlordship. Later he became an advisor and friend of Finrod Felagund, lord of Nargothrond, although the Falas remained independant. At the request of king Turgon of Gondolin, he built several messenger ships to sail to Valinor to request help from the Valar against Morgoth. All these missions failed, and only one survivor ever returned. After the havens of the Falas were destroyed, Círdan was instrumental in setting up the refuges at the Mouths of Sirion and the Isle of Balar, to which he retired. It was in this idle that he built the great ship Vingilot for Eärendil.
In the Second Age, Círdan stayed behind when the Elves were summoned to Valinor, and set up the havens of Forlond, Harlond and Mithlond in the destroyed land of Lindon (anciently Ossiriath). Círdan's exact status during that time is unknown, but it seems certain he served under Ereinion Gil-Galad, son of Fingon and last High King of the Noldor of Middle-earth. Círdan is mentioned as receiving the ships of the Númenóreans as they returned to the north of Middle-earth.
In the Third Age after the fall of Gil-galad and the beginning of the Age of Men, Círdan remained at the Grey Havens of Mithlond, and built ships which ferried the departing Elves to Valinor. Círdan had possession of the Great Ring Narya, rescued from Ereinion Gil-galad, but when the Istari or Wizards arrived in the early Third Age he recognised Olórin's wisdom, and gave him his ring. Círdan remained active behind the scenes, sending counsellors to the Grey Council at Rivendell, but his rôle in the War of the Ring ended when he sent away the ship that ferried across the other Ringbearers: Gandalf, Elrond, Galadriel, Bilbo, and Frodo, in the year 3021, end of the Third Age.