The availability of an environmental pool of symbionts and partner choice are crucial for the persistence of a mutualistic association with horizontally transmitted symbionts. In the deep-sea hydrothermal vent tubeworm Riftia pachyptila (Vestimentifera, Siboglinidae) it has been suggested that the Candidatus Endoriftia persephone symbiont is nearly monoclonal. Here, we show with high coverage metagenomics that Riftia pachyptila house a polyclonal symbiont population and that the dominant genotype shifts within adults. While juveniles share a specific dominant genotype also prevalent in vent biofilms and in adjacent benthic and pelagic deep-sea environments adults are dominated by varying genotypes. We propose that symbionts in juveniles reflect those on basalts because of direct uptake while changing abiotic conditions during host growth trigger symbiont shuffling. Our results suggest that there is a strong exchange between the free-living and symbiotic Endoriftia population, which is most likely caused by unselective partner choice during horizontal uptake of symbionts and the release of symbionts upon host death.