Abstract Although the costs of reproduction are predicted to vary with the quality of the breeding habitat thereby affecting population dynamics and life-history trade-offs, empirical evidence for this pattern remains sparse and equivocal. Costs of reproduction can operate through immediate ecological mechanisms or through delayed intrinsic mechanisms. Ignoring these separate pathways might hinder the identification of costs and the understanding of their consequences. We experimentally investigated the survival costs of reproduction for adult little owls (Athene noctua) within a gradient of habitat quality. We supplemented food to nestlings, thereby relieving the parents’ effort for brood provisioning. We used radio-tracking and Bayesian multi-state modelling based on marked recapture and dead recovery to estimate survival rates of adult little owls across the year as a function of food supplementation and habitat characteristics. Food supplementation to nestlings during the breeding season increased parental survival not only during the breeding season but also during the rest of the year. Thus, the low survival of parents of unfed broods likely represents both, strong ecological and strong intrinsic costs of reproduction. However, while immediate ecological costs occurred also in high quality habitats, intrinsic costs carrying over to the post-breeding period occurred only in low quality habitats. Our results suggest that immediate costs resulting from ecological mechanisms such as predation, are high also in territories of high habitat quality. Long-term costs resulting from intrinsic trade-offs, however, are only paid in low quality habitats. Consequently, differential effects of habitat quality on immediate ecological and delayed intrinsic mechanisms can mask the increase of costs of reproduction in low quality breeding habitats. Intrinsic costs may represent an underrated mechanism of habitat quality affecting adult survival rate thereby considerably accelerating population decline in degrading habitats. This study therefore highlights the need for a long-term perspective to fully assess the costs of reproduction and the role of habitat quality in modifying these costs.