Supergenes govern multi-trait-balanced polymorphisms in a wide range of systems; however, our understanding of their origins and evolution remains incomplete. The reciprocal placement of stigmas and anthers in pin and thrum floral morphs of distylous species constitutes an iconic example of a balanced polymorphism governed by a supergene, the distyly S -locus. Recent studies have shown that the Primula and Turnera distyly supergenes are both hemizygous in thrums, but it remains unknown whether hemizygosity is pervasive among distyly S -loci. As hemizygosity has major consequences for supergene evolution and loss, clarifying whether this genetic architecture is shared among distylous species is critical. Here, we have characterized the genetic architecture and evolution of the distyly supergene in Linum by generating a chromosome-level genome assembly of Linum tenue , followed by the identification of the S -locus using population genomic data. We show that hemizygosity and thrum-specific expression of S -linked genes, including a pistil-expressed candidate gene for style length, are major features of the Linum S -locus. Structural variation is likely instrumental for recombination suppression, and although the non-recombining dominant haplotype has accumulated transposable elements, S -linked genes are not under relaxed purifying selection. Our findings reveal remarkable convergence in the genetic architecture and evolution of independently derived distyly supergenes, provide a counterexample to classic inversion-based supergenes, and shed new light on the origin and maintenance of an iconic floral polymorphism. • The genome sequence of Linum tenue enabled the identification of the distyly supergene • The Linum distyly supergene harbors a 260-kb region unique to thrum individuals • The supergene is enriched for repeats and harbors a style-length candidate gene • Distyly supergenes exhibit convergent genetic architectures and evolution Gutiérrez-Valencia et al. identify the supergene that governs the iconic floral polymorphism of distyly in Linum. They show that the supergene harbors a 260-kb thrum-specific hemizygous region carrying a style-length candidate gene. These findings reveal striking convergence in the genetic architecture of independently evolved distyly supergenes. [ABSTRACT FROM AUTHOR]