Sexual compatibility in the Basidiomycota is governed by genetic identity at one or two loci, resulting in compatibility systems called bipolar and tetrapolar. The loci are known as HD and P/R, encoding homeodomain transcription factors and pheromone precursors and receptors, respectively. Bipolarity is known to evolve either by linkage of the two loci or by loss of mating-type determination of either the HD or the P/R locus. The ancestor to basidiomycete fungi is thought to have been tetrapolar, and many transitions to bipolarity have been described in different lineages. In the diverse genus Marasmius (Agaricales), both compatibility systems are found, and the system has been shown to follow the infrageneric sections of the genus, suggesting a single origin of bipolarity. Here, we tested this hypothesis using a comprehensive phylogenetic framework and investigated the mode by which bipolarity has evolved in this group. We utilized available genomic data and marker sequences to investigate evolution of sexual compatibility in Marasmius and allied genera. By generating a concatenated multilocus phylogeny, we found support for a single transition to known bipolarity within Marasmius. Furthermore, utilizing genomic data of the bipolar species Marasmius oreades, we found that the HD and P/R loci likely have remained unlinked through this transition. By comparing nucleotide diversity at the HD and P/R loci in Ma. oreades, we show that the HD locus has retained high diversity, and thus likely the function of determining sexual identity, as similarly in other bipolar mushroom-forming fungi. Finally, we describe the genomic architecture of the MAT loci of species of both sexual compatibility systems in Marasmiaceae and related families.