Development requires the coordinated action of many genes across space and time, yet numerous species are able to develop multiple discrete, alternate phenotypes. Such polymorphisms are often controlled by supergenes, sets of tightly-linked loci that function together to control development of a polymorphic phenotype. Although theories of supergene evolution are well established, the functional genetic differences between supergene alleles have been difficult to identify. The doublesex supergene controls mimicry polymorphism in several Papilio swallowtail butterflies, where divergent dsx alleles switch between discrete mimetic or non-mimetic female wing patterns. Here we show that the Papilio alphenor supergene evolved via recruitment of five new cis-regulatory elements (CREs) that control allele-specific dsx expression. Most dsx CREs, including three of the five new CREs, are bound by the DSX transcription factor itself. Additionally, DSX differentially binds a small number of unlinked CREs between mimetic and non-mimetic wings, suggesting that the supergene directly regulates expression of unlinked modifier genes that execute the mimetic development program. We thus identify the functional genetic elements of a supergene; propose that autoregulation provides a simple route to supergene origination and the evolution of dominance; and establish a molecular mechanism for epistasis between supergenes and their modifiers.