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Metapopulation dynamics can be shaped by foraging ecology, and thus be sensitive to shifts in prey availability. Genotyping 204 North Atlantic killer whales at 1346 loci, we investigated whether spatio-temporal population structuring is linked to prey type and distribution. Using population-based methods (reflecting evolutionary means), we report a widespread metapopulation connected across ecological groups based upon nuclear genome SNPs, yet spatial structuring based upon mitogenome haplotypes. These contrasting patterns of markers with maternal and biparental inheritance are consistent with matrilineal site fidelity and philopatry, and male-mediated gene flow among demes. Connectivity between fish-eating and 'mixed-diet' (eating both fish and mammal prey) killer whales, marks a deviation within a species renowned for its marked structure associated with ecology. However, relatedness estimates suggest distinct spatial clusters, and heterogeneity in recent gene flow between them. The contrasting patterns between inference of structure and inference of relatedness suggest that gene flow has been partially restricted over the past two to three generations (50-70 years). This coincides with the collapse of North Atlantic herring stocks in the late 1960s and the subsequent cessation of their seasonal connectivity. Statistically significant association between diet types and assignment of Icelandic killer whales to relatedness-based clusters indicated limited gene flow was maintained through Icelandic 'mixed-diet' whales when herring-mediated connectivity was diminished. Thus, conservation of dietary variation within this metapopulation is critical to ensure genetic health. Our study highlights the role of resource dynamics and foraging ecology in shaping population structure and emphasises the need for transnational management of this widespread migratory species and its prey., Competing Interests: Competing interests: The authors declare no conflicts of interests. Ethics: All samples from Greenland were collected under the research permits of the Greenland Institute of Natural Resources. Biopsies from Iceland were collected under an institutional permit of the Marine and Freshwater Research Institute., (© 2025. The Author(s).)