Repeated adaptive ecological diversification has commonly been reported in fish and has often been associated with trophic niche diversity. The main goal of this study was to investigate the extent of parallelism in the genomic and phenotypic divergence between piscivorous and planktivorous lake trout ecotypes from Laurentian Shield lakes, Canada. This was achieved by documenting the extent of morphological differentiation using geometric morphometrics and linear measurements as well as the pattern of genomic divergence by means of RADseq genotyping (3925 filtered SNPs) in 12 lakes. Our results indicate that the two ecotypes evolved distinct body shape and several linear measurements in parallel. Neutral genetic differentiation was pronounced between all isolated populations (Mean FST = 0.433), indicating no or very limited migration and pronounced genetic drift. Significant genetic differentiation also suggested partial reproductive isolation between ecotypes in the two lakes where they are found in sympatry. Combining different outlier detection methods, we identified 48 SNPs putatively under divergent selection between ecotypes, among which 10 could be annotated and related to functions such as developmental processes and ionic regulation. Finally, our results indicate that parallel morphological divergence is accompanied by both parallel and nonparallel genomic divergence, which is associated with the use of different trophic niches between ecotypes. The results are also discussed in the context of management and conservation of this highly exploited species throughout northern North America.