Recent ecotypic differentiation provides unique opportunities to investigate the genomic basis and architecture of local adaptation, while offering insights into how species form and persist. Sockeye salmon (Oncorhynchus nerka) exhibit migratory and resident (‘kokanee’) ecotypes, which are further distinguished into shore-spawning and stream-spawning reproductive ecotypes. Here, we analysed 36 sockeye (stream-spawning) and kokanee (stream- and shore-spawning) genomes from a system where they co-occur and have a recent common ancestry (Okanagan Lake/River in British Columbia, Canada) to investigate the genomic basis of reproductive and migratory behaviour. Examination of the genomic landscape of differentiation, differences in allele frequencies, and genotype-phenotype associations revealed three main blocks of sequence differentiation on chromosomes 7, 12, and 20, associated with migratory behaviour, spawning location, and spawning timing. Several structural variants identified in these same areas suggest they could contribute to ecotypic differentiation directly as causal variants or via maintenance of their genomic architecture through recombination suppression mechanisms. Genes in these regions were related to spatial memory and swimming endurance (SYNGAP, TPM3), as well as eye and brain development (including SIX6), potentially associated with differences in migratory behaviour and visual habitats across spawning locations, respectively. Additional genes (GREB1L, ROCK1) identified have been associated with timing of migration in other salmonids and could explain variation in timing of spawning in our study. Together, these results based on the joint analysis of sequence and structural variation represent a significant advance in our understanding of the genomic landscape of ecotypic differentiation at different stages in the speciation continuum.