The evolution of reproductive isolation in an ecological context may involve multiple facets of species divergence on which divergent selection may operate. These include variation in quantitative phenotypic traits, regulation of gene expression, and differential transmission of particular allelic combinations. Thus, an integrative approach to the speciation process involves identifying the genetic basis of these traits, in order to understand how they are affected by divergent selection in nature and how they ultimately contribute to reproductive isolation. In the Lake Whitefish (Coregonus clupeaformis), dwarf and normal species pairs sympatrically occur in several North American postglacial lakes. The limnetic dwarf whitefish distinguishes from its normal benthic relative by numerous life history, behavioural, morphological and gene expression traits, in relation with the exploitation of distinct ecological niches. Here, we have applied the RAD-Sequencing method to a hybrid backcross family to reconstruct a high-density genetic linkage map and perform QTL mapping in the Lake Whitefish. The 3061 cM map encompassed 3438 segregating RAD markers distributed over 40 linkage groups, for an average resolution of 0.89 cM. We mapped phenotypic and expression QTL underlying ecologically important traits as well as transmission ratio distortion QTL, and identified genomic regions harbouring clusters of such QTL. A narrow genomic region strongly associated with sex determination was also evidenced. Positional and functional information revealed in this study will be useful in ongoing population genomic studies to illuminate our understanding of the genomic architecture of reproductive isolation between whitefish species pairs.