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Over the last two decades the molecular phylogeny and classification of <i>Metarhizium</i> has been widely studied. Despite these efforts to understand this enigmatic genus, the basal lineages in <i>Metarhizium</i> are still poorly resolved. In this study, a phylogenetic framework is reconstructed for the <i>Clavicipitaceae</i> focusing on <i>Metarhizium</i> through increased taxon-sampling using five genomic loci (SSU, LSU, <i>tef, rpb1, rpb</i>2) and the barcode marker ITS rDNA. Multi-gene phylogenetic analyses and morphological characterisation of green-spored entomopathogenic <i>Metarhizium</i> isolates from Thailand and soil isolates of <i>M. carneum</i> and <i>M. marquandii</i> reveal their ecological, genetic and species diversity. Nineteen new species are recognised in the <i>Metarhizium</i> clade with narrow host ranges: two new species are found in the <i>M. anisopliae</i> complex - <i>M. clavatum</i> on <i>Coleoptera</i> larvae and <i>M. sulphureum</i> on <i>Lepidoptera</i> larvae; four new species are found in the <i>M. flavoviride</i> complex - <i>M. biotecense</i> and <i>M. fusoideum</i> on brown plant hoppers (<i>Hemiptera</i>), <i>M. culicidarum</i> on mosquitoes, <i>M. nornnoi</i> on <i>Lepidoptera</i> larvae; three new species <i>M. megapomponiae, M. cicadae, M. niveum</i> occur on cicadas; five new species <i>M. candelabrum, M. cercopidarum, M. ellipsoideum, M. huainamdangense M. ovoidosporum</i> occur on planthoppers, leafhoppers and froghoppers (<i>Hemiptera</i>); one new species <i>M. eburneum</i> on <i>Lepidoptera</i> pupae; and four new species <i>M. phuwiangense, M. purpureum, M. purpureonigrum, M. flavum</i> on <i>Coleoptera</i> <i>.</i> Of these 19 new species, seven produce a sexual morph (<i>M. clavatum, M. eburneum, M. flavum, M. phuwiangense, M. purpureonigrum, M. purpureum,</i> and <i>M. sulphureum</i>) and asexual morphs are found in the remaining new species and also in <i>M. sulphureum, M. purpureonigrum</i> and <i>M. purpureum. Metarhizium blattodeae, M. koreanum</i> and <i>M. viridulum</i> are new records for Thailand. An alternative neotype for <i>Metarhizium anisopliae</i> is proposed based on multi-gene and 5'<i>tef</i> analyses showing that CBS 130.71 from Ukraine is more suitable, being from a much closer geographical location to Metchnikoff's <i>Metarhizium anisopliae.</i> This isolate is distinct from the neotype of <i>Metarhizium anisopliae</i> var. <i>anisopliae</i> proposed by M. Tulloch from Ethiopia (ARSEF 7487). Six new genera are established for monophyletic clades subtending the core <i>Metarhizium</i> clade, including <i>Keithomyces, Marquandomyces, Papiliomyces, Purpureomyces, Sungia,</i> and <i>Yosiokobayasia. Metarhizium carneum, M. aciculare,</i> and <i>M. neogunnii</i> are combined in <i>Keithomyces</i> and one new combination for <i>M. marquandii</i> in <i>Marquandomyces</i> is proposed. <i>Purpureomyces</i> is introduced for species producing purple stromata including a new combination for <i>M. khaoyaiense</i> and two new species <i>P. maesotensis</i> and <i>P. pyriformis. Papiliomyces</i> contains two new combinations for <i>M. liangshanense</i> and <i>Metacordyceps shibinensis</i>. The genus <i>Sungia</i> is proposed for the Korean species <i>M. yongmunense</i> on <i>Lepidoptera</i> pupa and <i>Yosiokobayasia</i> for the Japanese species <i>M. kusanagiense</i> also on <i>Lepidoptera</i> pupa. A synoptic and dichotomous key to the accepted taxa is provided together with tables listing distinguishing morphological characters between species, host preferences, and geography.