The evolution of locally adapted phenotypes among populations that experience divergent selective pressures is a central mechanism for generating and maintaining biodiversity. Recently, the advent of high-throughput DNA sequencing technology has provided tools for investigating the genetic basis of this process in natural populations of non-model organisms. Kokanee, the freshwater form of sockeye salmon (Oncorhynchus nerka), occurs as two reproductive ecotypes, which differ in spawning habitat (tributaries vs. shorelines), however outside of the spawning season the two ecotypes co-occur in many lakes and lack diagnostic morphological characteristics. We used restriction site associated DNA (RAD) sequencing to identify 6,145 SNPs and genotype kokanee from multiple spawning sites in Okanagan Lake (British Columbia, Canada). Outlier tests revealed 18 loci putatively under divergent selection between ecotypes, all of which exhibited temporally stable allele frequencies within ecotypes. Six outliers were annotated to sequences in the NCBI database, two of which matched genes associated with early development. There was no evidence for neutral genetic differentiation, however, outlier loci demonstrated significant structure with respect to ecotype and had high assignment accuracy in mixed composition simulations. The absence of neutral structure combined with a small number of highly divergent outlier loci is consistent with theoretical predictions for the early stages of ecological divergence. These outlier loci were then applied to a realistic fisheries scenario in which additional RAD sequencing was used to genotype kokanee collected by trawl in Okanagan Lake, providing preliminary evidence that this approach may be an effective tool for conservation and management.