We studied the genetic architecture of the differences in the longevity between lines selected for postponed senescence and a control population of the seed beetle Acanthoscelides obtectus maintained on two hosts. By using lines with increased longevity, which were obtained by selection on natural variation in longevity, we showed that the genetic architecture of seed beetle longevity is complex, with sex-specific effects and variation attributable to many interacting genes, whose expression depend on the host on which the beetles were reared. The nonadditive genetic effects were more strongly expressed when reared on chickpeas, a novel host, than on beans. Outbreeding depression, with respect to longevity, was a consequence of both the intrinsic effect of interactions between genes from different parental sources (disruption of coadapted gene complexes) and the genotype × host interaction (loss of local adaptation).