Dispersing and non-dispersing individuals often differ in phenotypic traits (e.g. physiology, behaviour), but to what extent these differences are fixed or driven by external conditions remains elusive. We experimentally tested whether differences in nest-defence behaviour between dispersing and non-dispersing individuals changed with local habitat quality in collared flycatchers, by providing additional food during the nestling rearing period. In control (non-food-supplemented) nests, dispersers were less prone to defend their brood compared with non-dispersers, whereas in food-supplemented nests, dispersing and non-dispersing individuals showed equally strong nest defence. We discuss the importance of dispersal costs versus adaptive flexibility in reproductive investment in shaping these differences in nest-defence behaviour between dispersing and non-dispersing individuals. Irrespective of the underlying mechanisms, our study emphasizes the importance of accounting for environmental effects when comparing traits between dispersing and non-dispersing individuals, and in turn assessing the costs and benefits of dispersal.