Two commercially important scallop species of the genus Pecten are found in Europe: the north Atlantic Pecten maximus and the Mediterranean Pecten jacobaeus whose distributions abut at the Almeria-Orán front. Whilst previous studies have quantified genetic divergence between these species, the pattern of differentiation along the Pecten genome is unknown. Here, we mapped RADseq data from 235 P. maximus and 27 P. jacobaeus to a chromosome-level reference genome, finding a heterogeneous landscape of genomic differentiation. Highly divergent genomic regions were identified across 14 chromosomes, while the remaining five showed little differentiation. Demographic and comparative genomics analyses suggest that this pattern resulted from an initial extended period of isolation, which promoted divergence, followed by differential gene flow across the genome during secondary contact. Single nucleotide polymorphisms present within highly divergent genomic regions were located in areas of low recombination and contrasting patterns of LD decay were found between the two species, hinting at the presence of chromosomal inversions in P. jacobaeus. Functional annotations revealed that highly differentiated regions were enriched for immune-related processes and mRNA modification. While future work is necessary to characterize structural differences, this study provides new insights into the speciation genomics of P. maximus and P. jacobaeus.