Habitat fragmentation reduces the area of habitat patches and their connectedness in the landscape. It is well established that the level of connectedness impacts connectivity and metapopulation dynamics, and is therefore a central tenet in conservation biology. Connectedness equally generates sorting of phenotypes within the spatial network and therefore impacts local and regional eco-evolutionary dynamics. Paradoxically, recommendations for species conservation rely on principles derived from theory that neglects any individual phenotypic heterogenety and spatial organization.By creating experimental metapopulations using the model species Tetranychus urticae (two-spotted spider mite) with three levels of landscape connectedness and by regularly removing phenotypic structure in a subset of these populations, we tested the degree to which regional and local population dynamics are determined both by network connectedness and the phenotypic spatial organization.Our results show that some aspects of metapopulation dynamics can be attributed to the evolution of dispersal. More importantly, we find self-organization of phenotypic spatial structure to equalize the effects of reduced connectedness on metapopulation dynamics. These changes were all in the direction of improved metapopulation persistence. Contrary to expectations, the most connected local patches showed an overall reduced local population size, possibly originating from a faster depletion of resources from immigrants or transiting individuals.This experiment shows how metapopulation dynamics can significantly deviate from theoretical expectations if individual heterogeneity is considered, and more importantly that disruption of this phenotypic self-structuring may drive metapopulation dynamics towards higher risks of extinction.Significance StatementChanges in connectedness impact metapopulation dynamics but also the spatial organization of individual phenotypic heterogeneity. The extent to which metapopulation dynamics depend on this phenotypic structuring is unknown, despite the fact metapopulation theory is at the heart of conservation biology. By using experimental metapopulations and a randomization treatment, we demonstrate that the emerging spatial organization of individuals (both genetically and phenotypically) is a major driver of metapopulation dynamics. This spatial organization may be important as it may equalize all variation in metapopulation dynamics across a gradient of connectivity. This potentially rescuing effect stemming from the self-organization of phenotypes in metapopulations is of uttermost importance for conservation and translocation actions.