Understanding the dual roles of demographic and selective processes in the buildup of population divergence is one of the most challenging tasks in evolutionary biology. Here, we investigated the demographic history of Atlantic Salmon across the entire species range using 2035 anadromous individuals from North America and Eurasia. By combining results from admixture graphs, geo-genetic maps and an Approximate Bayesian Computation (ABC) framework, we validated previous hypotheses pertaining to secondary contact between European and Northern American populations, but also identified secondary contacts in European populations from different glacial refugia. We further identified the major sources of admixture from the southern range of North America into more northern populations along with a strong signal of secondary gene flow between genetic regional groups. We hypothesize that these patterns reflects the spatial redistribution of ancestral variation across the entire North American range. Results also support a role for linked selection and differential introgression that likely played an under-appreciated role in shaping the genomic landscape of species in the Northern hemisphere. We conclude that studies between partially isolated populations should systematically include heterogeneity in selective and introgressive effects among loci to perform more rigorous demographic inferences of the divergence process.