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A six-gene phylogeny of the Inocybaceae is presented to address classification of major clades within the family. Seven genera are recognized that establish a global overview of phylogenetic relationships in the Inocybaceae. Two genera-<i>Nothocybe</i> and <i>Pseudosperma-</i>are described as new. Two subgenera of <i>Inocybe</i>-subg. <i>Inosperma</i> and subg. <i>Mallocybe-</i>are elevated to generic rank. These four new genera, together with the previously described <i>Auritella, Tubariomyces</i>, and now <i>Inocybe</i> sensu stricto, constitute the Inocybaceae, an ectomycorrhizal lineage of Agaricales that associates with at least 23 plant families worldwide. <i>Pseudosperma, Nothocybe</i>, and <i>Inocybe</i> are recovered as a strongly supported inclusive clade within the family. The genus <i>Nothocybe</i>, represented by a single species from tropical India, is strongly supported as the sister lineage to <i>Inocybe</i>, a hyperdiverse genus containing hundreds of species and global distribution. Two additional inclusive clades, including <i>Inosperma, Tubariomyces, Auritella</i>, and <i>Mallocybe</i>, and a nested grouping of <i>Auritella, Mallocybe</i>, and <i>Tubariomyces</i>, are recovered but with marginal statistical support. Overall, the six-gene data set provides a more robust phylogenetic estimate of relationships within the family than do single-gene and single-gene-region estimates. In addition, Africa, India, and Australia are characterized by the most genera in the family, with South America containing the fewest number of genera. A total of 180 names are recombined or proposed as new in <i>Inosperma, Mallocybe</i>, and <i>Pseudosperma</i>. A key to genera of Inocybaceae is provided.