The spatial dispersal of individuals plays an important role in the dynamics of populations, and is central to metapopulation theory. Dispersal provides connections within metapopulations, promoting demographic and evolutionary rescue, but may also introduce maladapted individuals, potentially lowering the fitness of recipient populations through introgression of heritable traits. To explore this dual nature of dispersal, we modify a well-established eco-evolutionary model of two locally adapted populations and their associated mean trait values, to examine recruiting salmon populations that are connected by density-dependent dispersal, consistent with collective migratory behaviour that promotes navigation. When the strength of collective behaviour is weak such that straying is effectively constant, we show that a low level of straying is associated with the highest gains in metapopulation robustness and that high straying serves to erode robustness. Moreover, we find that as the strength of collective behaviour increases, metapopulation robustness is enhanced, but this relationship depends on the rate at which individuals stray. Specifically, strong collective behaviour increases the presence of hidden low-density basins of attraction, which may serve to trap disturbed populations, and this is exacerbated by increased habitat heterogeneity. Taken as a whole, our findings suggest that density-dependent straying and collective migratory behaviour may help metapopulations, such as in salmon, thrive in dynamic landscapes. Given the pervasive eco-evolutionary impacts of dispersal on metapopulations, these findings have important ramifications for the conservation of salmon metapopulations facing both natural and anthropogenic contemporary disturbances.