Summary Heterostyly, a plant sexual polymorphism controlled by the S ‐locus supergene, has evolved numerous times among angiosperm lineages and represents a classic example of convergent evolution in form and function. Determining whether underlying molecular convergence occurs could provide insights on constraints to floral evolution. Here, we investigated S ‐locus genes in distylous Gelsemium (Gelsemiaceae) to determine whether there is evidence of molecular convergence with unrelated distylous species. We used several approaches, including anatomical measurements of sex‐organ development and transcriptome and whole‐genome sequencing, to identify components of the S ‐locus supergene. We also performed evolutionary analysis with candidate S ‐locus genes and compared them with those reported in Primula and Turnera . The candidate S ‐locus supergene of Gelsemium contained four genes, of which three appear to have originated from gene duplication events within Gelsemiaceae. The style‐length genes GeCYP in Gelsemium and CYP734A50 in Primula likely arose from duplication of the same gene, CYP734A1 . Three out of four S ‐locus genes in Gelsemium elegans were hemizygous, as previously reported in Primula and Turnera . We provide genomic evidence on the genetic convergence of the supergene underlying distyly among distantly related angiosperm lineages and help to illuminate the genetic architecture involved in the evolution of heterostyly.