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Aim: We assessed the population genetic structure of the kleptoparasitic spider Argyrodes bonadea across the Southwestern Pacific islands. Our aim is to evaluate the impact of overseas distances and, in particular, the Kerama gap, as potential drivers of genetic differentiation. If no relationship exists, then we assume dispersal following adaptive change as alternative non‐vicariant mechanism that generates divergence. Location: Southwestern Pacific Islands. Taxon: Argyrodes bonadea. Methods: We used mitochondrial Cytochrome Oxidase 1 (CO1) gene sequences and Restriction Site‐associated DNA Sequencing (RAD‐seq) for our analyses. Results: Two strongly supported lineages, an Amami‐Okinawa Lineage (AOL) and an Austral‐Asia Lineage (AAL), correspond to two separate clades, roughly divided by the Kerama Gap, in phylogenetic trees estimated here. However, species delimitation led to the interpretation of only a single species present. The AOL exhibits complex, geographically structured host web spider species specificity, wherein the Amami population utilizes Cyrtophora, but AOL samples in Okinawa associate exclusively with Nephila—and yet all broadly distributed AAL populations show no evidence of host web spider species specificity. Main Conclusion: The population boundary between AOL and AAL likely results from local adaptation to novel hosts—instead of isolation by the Kerama Gap—following long‐distance dispersal and range expansion. Our results suggest kleptoparasitic spiders have the capacity to overcome permanent deep‐sea barriers and colonize distant landmasses. Whereas peripheral populations (AOL) demonstrate the capacity for specialization to a single host, which may have contributed to genetic differentiation and isolation, the broadly distributed AAL persists and has successfully expanded its geographical range as a host generalist, which may contribute to ongoing gene flow inferred in this study. [ABSTRACT FROM AUTHOR]