Local extirpations and extreme bottlenecks can deplete genetic variation and obscure population dynamics, especially in highly mobile species. The gray whale (Eschrichtius robustus) undertakes some of the longest known migrations among mammals, and conventional wisdom acknowledges two stocks (eastern and western gray whales) in the Pacific. Commercial whaling depleted both stocks, and while the Eastern North Pacific (ENP) stock has rebounded, the western stock was feared extirpated. In the post-whaling era, the origin of a small summer aggregation near Sakhalin Island, Russia (which we refer to as the Western North Pacific (WNP) stock) is unclear; this group may include descendants from the original western stock, founders from the eastern stock, or some combination of the two. To clarify the genetic affinities of WNP gray whales, we generated whole genome resequencing data for 74 individuals sampled from both geographic regions to assess their origins. Surprisingly, WNP whales are more genetically varied than ENP whales according to principal components and admixture analyses. We present evidence that this structure is due to mixed ancestry in WNP, with admixture occurring between historical eastern and western stocks. Genomic signals based on both single nucleotide polymorphisms and on copy number variants indicate that despite mixed ancestry, the influx of eastern gene flow has largely homogenized genomic diversity across the Pacific. These findings highlight the ability of whole-genome data to help resolve questions of extirpation and to clarify complex gene flow dynamics in highly mobile species.