Background Theory predicts that lower dispersal, and associated gene flow, leads to decreased genetic diversity in small isolated populations, which generates adverse consequences for fitness, and subsequently for demography. Here we report for the first time this effect in a well-connected natural butterfly metapopulation with high population densities at the edge of its distribution range. Results We demonstrate that: (1) lower genetic diversity was coupled to a sharp decrease in adult lifetime expectancy, a key component of individual fitness; (2) genetic diversity was positively correlated to the number of dispersing individuals (indicative of landscape functional connectivity) and adult population size; (3) parameters inferred from capture-recapture procedures (population size and dispersal events between patches) correlated much better with genetic diversity than estimates usually used as surrogates for population size (patch area and descriptors of habitat quality) and dispersal (structural connectivity index). Conclusion Our results suggest that dispersal is a very important factor maintaining genetic diversity. Even at a very local spatial scale in a metapopulation consisting of large high-density populations interconnected by considerable dispersal rates, genetic diversity can be decreased and directly affect the fitness of individuals. From a biodiversity conservation perspective, this study clearly shows the benefits of both in-depth demographic and genetic analyses. Accordingly, to ensure the long-term survival of populations, conservation actions should not be blindly based on patch area and structural isolation. This result may be especially pertinent for species at their range margins, particularly in this era of rapid environmental change.