Various infrageneric classifications of the genus Geastrum have been proposed, all of them exclusively based on morphology. They are highly divergent due to the different relative value that each author gave to particular morphological features. There is no consensus about any of these classifications, and therefore most modern studies avoid classifying Geastrum species in supraspecific units. Here, a new subdivision of the genus Geastrum is presented, based on phylogenetic analyses of four molecular markers, viz., 5.8S nrDNA, nrLSU, rpb1, and atp6. This classification is also supported by chemical reactions with syringaldazine and guiaiac gum, and by some morphological characters. Most reliable morphological characters include both classically studied features (e.g., endoperidial surface, peristome structure, mycelial layer), and recently discovered ones (e.g., rhizomorph crystals). Previously published infrageneric classifications are reviewed, showing many discrepancies with the phylogenetic data. A new infrageneric subdivision is proposed: sect. Campestria sect. nov., sect. Corollina sect. nov. (including subsect. Lageniformia subsect. nov., subsect. Marginata, and subsect. Plicostomata), sect. Elegantia sect. nov., sect. Exareolata, sect. Fimbriata, sect. Fornicata, sect. Geastrum (including subsect. Arenaria subsect. nov., subsect. Geastrum, subsect. Quadrifida subsect. nov., and subsect. Sulcostomata), sect. Hariotia sect. nov., sect. Hieronymia sect. nov., sect. Myceliostroma (including subsect. Epigaea and subsect. Velutina subsect. nov.), sect. Papillata, sect. Pseudolimbata sect. nov., sect. Schmidelia sect. nov., and sect. Trichaster. The phylogenetic and morphological boundaries among three genera of Geastraceae, viz., Geastrum, Myriostoma, and Radiigera, are also evaluated. Myriostoma likely represents a different phylogenetic lineage within Geastraceae and is confirmed as distinct from Geastrum. However, Radiigera is nested in Geastrum, and therefore it is confirmed as a synonym of Geastrum.