Regions of the genome displaying elevated differentiation (genomic islands of divergence) are thought to play an important role in local adaptation, especially in populations experiencing high gene flow. However, the characteristics of these islands as well as the functional significance of genes located within them remain largely unknown. Here, we used data from thousands of SNPs aligned to a linkage map to investigate genomic islands of divergence in three ecotypes of sockeye salmon (Oncorhynchus nerka) from a single drainage in southwestern Alaska. We found ten islands displaying high differentiation among ecotypes, contrasting neutral structure throughout the rest of the genome which was low and not partitioned by ecotype. One island on linkage group 13 was particularly large and contained six SNPs with FST > 0.14 (average FST of neutral SNPs = 0.01). Functional annotation revealed that the peak of this island contained a non-synonymous mutation in a gene involved in growth in other species (TULP4). The islands that we discovered were relatively small (80 - 402 Kb), loci found in islands did not show reduced levels of diversity, and loci in islands displayed slightly elevated linkage disequilibrium. These attributes suggest that the islands discovered here were likely generated by divergence hitchhiking, however, we cannot rule out the possibility that other mechanisms may have produced them. Our results suggest that islands of divergence serve an important role in local adaptation with gene flow and represent a significant advance towards understanding the genetic basis of ecotypic differentiation.