Historical patterns of dispersal and population isolation are key components shaping contemporary genetic diversity across landscapes and require explicit consideration when examining the relative role of different factors in driving the evolution of host specificity in parasitic organisms. In this study, we investigate the worldwide colonisation history of a common ectoparasite of seabirds, the tick Ixodes uriae. This tick has a circumpolar distribution across both hemispheres, but has repeatedly formed host-specific races within different regions. By combining mitochondrial and nuclear data, we infer how this species spread to its present-day distribution and how the colonisation process has affected the geographic and host-associated structure of this tick within regions. We demonstrate that I. uriae is highly structured and isolates into four genetic groups that correspond to well-defined geographical regions. Molecular dating suggests that the diversification of I. uriae began in the early Miocene (22 Myr) and that this tick colonised most of the Southern hemisphere before moving into northern latitudes via two independent routes. However, no relationship between the degree of host race divergence and colonisation history was evident, supporting previous hypotheses that host specialization evolves relatively rapidly in this parasite, but does not typically lead to speciation. We discuss the possible historical and contemporary mechanisms of large scale dispersal for this ectoparasite and how its biological characteristics may condition current patterns of genetic diversity. More generally, our results illustrate how combining broad-scale sampling and modern molecular tools can help disentangle complex patterns of diversification in widespread parasites.