Ecological interactions are an important source of rapid evolutionary change and thus may generate a significant portion of novel biodiversity. Such changes may be particularly prevalent in parasites, where hosts can induce strong selection for adaptation. To understand the relative frequency at which host-associated divergences occur, it is essential to examine the evolutionary history of the divergence process, particularly when it is occurring over large geographical scales where both geographical and host-associated isolation may playa part. In this study, we use population genetics and phylogeography to study the evolutionary history of host-associated divergence in the seabird tick Ixodes uriae (Acari, Ixodidae). We compare results from microsatellite markers that reflect more ecological timescales with a conserved mitochondrial gene (COIII) that reflects more ancient divergence events. Population structure based on microsatellites showed clear evidence of host-associated divergence in all colonies examined. However, isolated populations of the same host type did not always group together in overall analyses and the genetic differentiation among sympatric host races was highly variable. In contrast, little host or geographical structure was found for the mitochondrial gene fragment. These results suggest that host race formation in I. uriae is a recent phenomenon, that it may have occurred several times and that local interactions are at different points in the divergence process. Rapid divergence in I. uriae implies a strong interaction with its local host species, an interaction that will alter the ecological dynamics of the system and modify the epidemiological landscape of circulating micropathogens.