The maintenance of species integrity despite pervasive hybridization is ruled by the interplay between reproductive barriers. Endogenous postzygotic isolation will shape the patterns of introgression in hybrid zones, leading to variable outcomes depending on the genetic mechanism involved. Here, we analysed experimental and natural hybrid populations of Aegilops geniculata and Aegilops triuncialis to examine the genetics of species boundaries in the face of gene flow. Because long-terminal repeat retrotransposons (LTR-RTs) showing differential evolutionary trajectories are probably to affect hybrid dysgenesis and reproductive isolation between these wild wheat species, we addressed the impact of LTR-RTs in shaping introgression between them. Experimental settings involving artificial sympatry and enforced crossings quantified strong, but incomplete reproductive isolation, and highlighted asymmetrical endogenous postzygotic isolation between the two species. Natural hybrid zones located in the northern Golan Heights were analysed using plastid DNA, amplified fragment length polymorphisms (AFLP) marking random sequences, and sequence-specific amplified polymorphisms (SSAP) tracking insertions from six LTR-RT families. This analysis demonstrated asymmetrical introgression and genome reorganization. In comparison with random sequences and quiescent LTR-RTs, those LTR-RTs predicted to be activated following conflicting interactions in hybrids revealed differential introgression across the hybrid zones. As also reported for synthetic F1 hybrids, such LTR-RTs were specifically reorganized in the genomes of viable hybrids, confirming that conflicts between selfish LTR-RTs may represent key incompatibilities shaping species boundaries and fostering long-term species integrity in the face of gene flow.