Species limits in the small genus Geopyxis are debatable because of problems with interpreting the few phenotypic features and poor documentation of types. To clarify species boundaries and diversity, we studied the morphology of 74 specimens of Geopyxis from the Northern Hemisphere, including five types, and sequenced four loci for 57 representatives: the nuc rDNA ITS1-5.8S-ITS2 (ITS), D1-D2 domains of nuc 28S rDNA (28S), translation elongation factor (tef1), and (or) part of the second largest subunit of the RNA polymerase II (rpb2) (5–7 region). Eight species are delimited. Six species are shown to be highly supported as reciprocally monophyletic: G. aleurioides sp. nov., G. alpina s. l., G. carbonaria, G. delectans, G. korfii, and G. majalis. In addition, coalescent-based Bayesian species delimitation shows G. alpina s. l. constitutes three cryptic species: G. alpina s. str., G. deceptiva sp. nov., and G. rehmii. ITS-28S sequences of type material show that G. vulcanalis and G. foetida are synonyms of G. carbonaria. A lectotype is designated for Humaria delectans and the name is combined in Geopyxis. Morphological characters that can be used to distinguish Geopyxis species are presence/absence of a long stipe, spore size and shape, and pigmented resinous exudates in medullary and ectal excipulum. Geopyxis carbonaria and G. delectans produce apothecia almost exclusively on burned ground. Bayesian analyses detected highly supported conflicts among different loci regarding generic delimitation and species relationships. Two hypogeous genera, Stephensia and Hydnocystis, are confirmed to nest within Geopyxis. The relationships between species of Geopyxis and Tarzetta, Stephensia shanorii and Paurocotylis pila, are unresolved. Six out of eight species of Geopyxis recognized in this study have intercontinental disjunct distributions.