In many species, individuals can develop into strikingly different morphs, which are determined by a simple Mendelian locus. How selection shapes loci that control complex p henotypic differences remains poorly understood. In the spider gibbosus, males either develop into a ‘hunched’morph with conspicuous head structures or as a fast developing ‘flat’morph with a female- like appearance. We show that the hunched differs from the f lat-determinin g allele by a hunch-specific genomic fragment of approximately 3 megabases. This fragment comprises dozens of genes that duplicated from genes found at different chromosomes. All functional duplicates, including doublesex- a key sexual differentiation regulatory gene, show male-specific expression, which il lustrates their combined role as a masculinizing supergene. Our findings demonstrate how extensive indel polymorphisms and duplications of regulatory genes may contribute to t he evolution of co-adapted gene clusters, sex-limi ted reproductive morphs, and the enigmatic evolution of exaggerated sexual traits in general.