The origin of a new diploid species by means of hybridization requires the successful merger of differentiated parental species’ genomes. To study this process, the genomic composition of three experimentally synthesized hybrid lineages was compared with that of an ancient hybrid species. The genomic composition of the synthesized and ancient hybrids was concordant (r(s) = 0.68, P < 0.0001), indicating that selection to a large extent governs hybrid species formation. Further, nonrandom rates of introgression and significant associations among unlinked markers in each of the three synthesized hybrid lineages imply that interactions between coadapted parental species’ genes constrain the genomic composition of hybrid species.