Understanding how new species arise through the progressive establishment of reproductive isolation (RI) barriers between diverging populations is a major goal in Evolutionary Biology. An important result of speciation genomics studies is that genomic regions involved in RI frequently harbor anciently diverged haplotypes that predate the reconstructed history of species divergence. The possible origins of these old alleles remain much debated, as they relate to contrasting mechanisms of speciation that are not yet fully understood. In the European sea bass (Dicentrarchus labrax), the genomic regions involved in RI between Atlantic and Mediterranean lineages are enriched for anciently diverged alleles of unknown origin. Here, we used haplotype-resolved whole-genome sequences to test whether divergent haplotypes could have originated from a closely related species, the spotted sea bass (Dicentrarchus punctatus). We found that an ancient admixture event betweenD. labraxandD. punctatusis responsible for the presence of shared derived alleles that segregate at low frequencies in both lineages ofD. labrax. An exception to this was found within regions involved in RI between the twoD. labraxlineages. In those regions, archaic tracts originating fromD. punctatuslocally reached high frequencies or even fixation in Atlantic genomes but were almost absent in the Mediterranean. We showed that the ancient admixture event most likely occurred betweenD. punctatusand theD. labraxAtlantic lineage, while Atlantic and MediterraneanD. labraxlineages were experiencing allopatric isolation. Our results suggest that local adaptive introgression and/or the resolution of genomic conflicts provoked by ancient admixture have probably contributed to the establishment of RI between the twoD. labraxlineages.