A fragmented habitat becomes increasingly fragmented for species at higher trophic levels, such as parasitoids. To persist, these species are expected to possess life-history traits, such as high dispersal, that facilitate their ability to use resources that become scarce in fragmented landscapes. If a specialized parasitoid disperses widely to take advantage of a sparse host, then the parasitoid population should have lower genetic structure than the host. We investigated the temporal and spatial genetic structure of a hyperparasitoid (fourth trophic level) in a fragmented landscape over 50 × 70 km, using microsatellite markers, and compared it with the known structures of its host parasitoid, and the butterfly host which lives as a classic metapopulation. We found that population genetic structure decreases with increasing trophic level. The hyperparasitoid has fewer genetic clusters (K = 4), than its host parasitoid (K = 15), which in turn is less structured than the host butterfly (K = 27). The genetic structure of the hyperparasitoid also shows temporal variation, with genetic differentiation increasing due to reduction of the population size, which reduces the effective population size. Overall, our study confirms the idea that specialized species must be dispersive to use a fragmented host resource, but that this adaptation has limits.