Species such as threespine stickleback fish that are distributed across landscapes with divergent selective environments and that have diversified on different time scales can be valuable for understanding evolutionary processes. Here we synthesize high resolution genotypic and phenotypic data to explore a largely unstudied distribution of threespine stickleback populations living in marine and freshwater habitats along coastal and inland regions of northwestern Oregon. Because many inland aquatic habitats of Oregon were not glaciated during the last ice age, we hypothesized that some extant Oregon lake and river stickleback are descended from freshwater populations that were established long before the well-studied, post-glacial freshwater populations of Alaska. Here we characterize the major phenotypic and genetic axes of differentiation in Oregon stickleback, and compare these patterns to their Alaska counterparts currently inhabiting regions that were covered by ice during the last glacial maximum. Phenotypic variation in Oregon stickleback is predictably partitioned between oceanic and freshwater habitats. However, we also found that genetic divergence in Oregon ecotypes is much greater than divergence among studied stickleback populations in Alaska. Additionally, we report a surprising phenotypic and genetic affinity between oceanic stickleback with freshwater populations that live far inland in two Oregon river basins.