Technical Abstract: Intraspecific variability in social organization is common, yet the underlying causes are rarely known1-3. In the fire ant Solenopsis invicta, the existence of two divergent forms of social organisation is under the control of a single Mendelian genomic element marked by two variants of an odorant binding protein (OBP) gene4-8. Here we characterize the genomic region responsible for this important social polymorphism and show that it is part of a pair of heteromorphic chromosomes having many of the key properties of sex chromosomes. The two variants, hereafter referred as the Social B and Social b (SB and Sb) chromosomes, are characterized by a largeregion of ca. 13 Mb (55% of the chromosome) where recombination is completely suppressed between SB and Sb. Recombination appears to occur normally between the SB chromosomes but is impossible between Sb chromosomes because Sb/Sb individuals are non-viable. Genomic comparisons revealed limited differentiation between SB and Sb, with all or at least the vast majority of the 616 genes identified in the non-recombining region present in the two variants. The reduced recombination between the two heteromorphic Social chromosomes can be explained at least partly by the increased number of repetitive elements and insertions in the non-recombining region of Sb compared with the homologous region of SB.Moreover, we identified an inversion on the Sb chromosome, which may further suppress recombination. Importantly, the non-recombining region comprises most of the genes with demonstrated expression differences between individuals of the two social forms. These findings highlight how genomic rearrangements can maintain divergent adaptive social phenotypes involving many genes acting in concert by locally limiting recombination.