Understanding the genomic relationship between wild and cultivated genomes would facilitate access to the untapped variability found in crop wild relatives. We developed genome assemblies of a cultivated lentil (Lens culinaris) as well as a wild relative (L. ervoides). Comparative analyses revealed large-scale structural rearrangements and additional repetitive DNA in the cultivated genome, resulting in regions of reduced recombination, segregation distortion and permanent heterozygosity in the offspring of a cross between the two species. These novel findings provide plant breeders with better insight into how best to approach accessing the novel variability available in wild relatives.