Understanding how genetic variation is partitioned across genomes within and among populations is a fundamental problem in ecological and evolutionary genetics. To address this problem we are studying the threespine stickleback fish, which has repeatedly undergone parallel phenotypic and genetic differentiation when oceanic fish have invaded freshwater habitats. While significant evolutionary genetic research has been performed using stickleback from geographic regions that have been de-glaciated in the last 20,000 years, less research has focused on freshwater populations that predate the last glacial maximum. We are performing RAD-seq based population genomic analyses on stickleback from across Oregon, which was not glaciated during the last maximum. These stickleback populations may be significantly older than those in recently de-glaciated regions and harbor different genetic variation and genomic architectures. We sampled stickleback from coastal, Willamette Basin, and central Oregon sites, analyzed their genetic diversity using RAD-seq, performed STRUCTURE analyses and reconstructed their phylogeographic history, and tested the hypothesis of recent stickleback introduction into central Oregon, where incidence of this species was only recently documented. Our results show a clear phylogeographic break between coastal and inland populations, with oceanic populations exhibiting the lowest levels of divergence from one another. Our data also clearly show that the Willamette Basin and central Oregon populations form a clade of closely related populations, a finding consistent with a recent introduction of stickleback into central Oregon. Finally, genome wide analysis of genetic diversity (p) and correlations of alleles within individuals in subpopulations (FIS) support a role for introgressive hybridization in coastal populations and a recent expansion in eastern Oregon. Our results exhibit the power of next generation sequencing genomic approaches such as RAD-seq to identify both historical population structure and recent colonization history.