Parasitic plants depend on other plants for nutrients and water and have undergone evolutionary processes tightly linked to their host range. As parasitic adaptations specialise host range, host shifts between parasite lineages are considered essential events that can lead to genetic differentiation and speciation. A thorough examination of population genealogy covering the entire host range is imperative to comprehend the impact of host-shift evolution on parasitic plant species diversity. Therefore, we investigated the population genetic structure of Orobanche boninsimae (Orobanchaceae), an endemic parasitic plant in the Bonin (Ogasawara) Islands. The host species of O. boninsimae are entirely distinct from those of other Orobanche species and show differences between geographically isolated islands, even though the host species coexist in some localities. Genetic differentiation was observed among populations from different islands, corresponding to variations in the host range of O. boninsimae. Demographic analysis supported a scenario in which populations on the southern island emerged through the admixture of populations parasitic on the different host species from the northern islands. This suggests a progressive colonisation process, wherein continental ancestors established in the northern islands underwent a host shift, followed by the migration of a lineage to the southern island. Notably, host shift across islands may have occurred through the admixture of populations. These findings provide a foundation for elucidating the roles of host plants and geographical isolation in the speciation of parasitic plants and enhance our understanding of the mechanisms driving parasitic plant diversification.