Despite the biological importance and diversity of nematodes, little is known of the factors influencing their dispersal and shaping their evolutionary history. Populations of the cosmopolitan species Pristionchus pacificus are characterized by high genetic diversity and strong spatial structure, which contrasts with patterns detected in nematode species such as Caenorhabditis elegans. The environmentally heterogeneous volcanic Mascarene Islands provide an ideal setting for investigating fine-scale patterns of nematode migration and gene flow. Based on the analysis of data from 19 nuclear microsatellites and one mitochondrial marker, we infer support for the colonization of both La Réunion Island and Mauritius from similar multiple geographical sources. Although the long-term persistence of populations on both islands is well supported, the historical colonization of one island from the other cannot be discounted. In fact, periodic, bi-directional migration between the islands following their initial colonization is strongly supported in isolation with migration analyses, supporting the occurrence of rare trans-oceanic dispersal events in P. pacificus. Through a combination of population and landscape genetic analyses we also infer non-uniform dispersal across the landscape on the island of La Réunion, probably mediated by the movements of beetle hosts. Collectively, we show that gene flow in P. pacificus is limited by environmental and oceanic barriers, and shaped by the intricacies of the nematode–beetle host interaction