The genomic shock hypothesis stipulates that the stress associated with divergent genomes admixture can cause transposable elements (TEs) derepression which could act as a strong postzygotic isolation mechanism. TEs impact gene structure, expression patterns and chromosome organization, and may have deleterious consequences when released. For this reason, they are silenced by heterochromatin formation, which includes DNA methylation. Here we show that a significant proportion of TEs are differentially methylated between the ‘Dwarf’ (limnetic) and the ‘Normal’ (benthic) whitefish, two nascent species that diverged some 15,000 generations ago within the Coregonus clupeaformis (complex). Moreover, TEs are overrepresented among sites that were demethylated in F1 hybrids, indicative of their derepression, consistent with earlier studies that revealed TE transcriptional derepression causing abnormal embryonic development and death of hybrids. Our results support the hypothesis of a genomic shock in dwarf-normal whitefish hybrids causing methylation reprogramming and TE derepression which act as a mechanism off postzygotic isolation.