Polymorphic species are useful models for investigating the evolutionary processes driving diversification. Such processes include colonization history as well as contemporary selection, gene flow, and genetic drift, which can vary between intraspecific morphs as a function of their distinct life histories. The interactive and relative influence of such evolutionary processes on morph differentiation critically informs morph-specific management decisions and our understanding of incipient speciation. We therefore investigated how geographic distance, environmental conditions, and colonization history interacted with morph migratory capacity in the highly polymorphic fish species, Arctic Charr (Salvelinus alpinus). Using an 87k SNP chip we genetically characterized recently evolved anadromous, resident, and landlocked charr collected from 45 locations across a secondary contact zone of three charr glacial lineages in eastern Canada. A strong pattern of isolation by distance across all populations suggested geographic distance principally shaped genetic structure. Landlocked populations had lower genetic diversities and higher genetic differentiation than anadromous populations. However, genetic diversity was generally temporally stable in landlocked populations in comparison to recent decreases in anadromous populations. Genetic diversity positively correlated with latitude, potentially indicating southern anadromous populations’ vulnerability to climate change and greater introgression between the Arctic and Atlantic glacial lineages in northern Labrador. Local adaptation was suggested by the observation of several environmental variables strongly associating with functionally relevant outlier genes including a region on chromosome AC21 potentially associated with anadromy. Our results demonstrate that gene flow, colonization history, and local adaptation uniquely interact to influence the genetic variation and evolutionary trajectory of populations.