The parallel evolution of nascent pairs of ecologically differentiated species offers an opportunity to get a better glimpse at the genetic architecture of speciation. Of particular interest is our recent ability to consider a wider range of genomic variants, not only single-nucleotide polymorphisms (SNPs), thanks to long-read sequencing technology. We can now identify structural variants (SVs) like insertions, deletions, and other structural rearrangements, allowing further insights into the genetic architecture of speciation and how different variants are involved in species differentiation. Here, we investigated genomic patterns of differentiation between sympatric species pairs (Dwarf and Normal) belonging to the Lake Whitefish (Coregonus clupeaformis) species complex. We assembled the first reference genomes for both Dwarf and Normal Lake Whitefish, annotated the transposable elements, and analysed the genome in the light of related coregonid species. Next, we used a combination of long-read and short-read sequencing to characterize SVs and genotype them at population-scale using genome-graph approaches, showing that SVs cover five times more of the genome than SNPs. We then integrated both SNPs and SVs to investigate the genetic architecture of species differentiation in two different lakes and highlighted an excess of shared outliers of differentiation. In particular, a large fraction of SVs differentiating the two species was driven by transposable elements (TEs), suggesting that TE accumulation during a period of allopatry predating secondary contact may have been a key process in the speciation of the Dwarf and Normal Whitefish. Altogether, our results suggest that SVs play an important role in speciation and that by combining second and third generation sequencing we now have the ability to integrate SVs into speciation genomics.