Dispersal, whether in the form of a dandelion seed drifting on the breeze, or a salmon migrating upstream to breed in a non-natal stream, transports genes between locations. At these locations, local adaptation modifies the gene frequencies so their carriers are better suited to particular conditions, be those of newly disturbed soil or a quiet river pool. Both dispersal and local adaptation are major drivers of population structure; however, in general, their respective roles are not independent and the two may often be at odds with one another evolutionarily, each one exhibiting negative feedback on the evolution of the other. Here we investigate their joint evolution within a simple discrete-time, metapopulation model. Depending on environmental conditions, their evolutionary interplay leads to either a monomorphic population of highly dispersing generalists or a rarely dispersing, locally adapted, polymorphic population, each adapted to a particular habitat type. A critical value of environmental heterogeneity divides these two selection regimes and the nature of the transition between them is determined by the level of kin competition. When kin competition is low, at the transition we observe discontinuities, bistability and hysteresis in the evolved strategies; however, when high, kin competition moderates the evolutionary feedback and the transition is smooth.