Three new species of the fungus-growing ant genus Myrmicocrypta Fr. Smith are described from Brazil and Peru, all unique within the genus due to their shared character state of erect pilosity. Myrmicocrypta erectapilosa sp. nov. and Myrmicocrypta bucki sp. nov. are otherwise typical for the genus in their small size and effaced, tuberculate sculpture, whereas Myrmicocrypta camargoi sp. nov. is also unique in its large size and pronounced sculpture. M. erectapilosa and M. bucki are closely related but can be distinguished by differences in the frontoclypeal and hypostomal teeth, frontal lobes, mesonotal sculpture, and propodeal spines. All castes (workers, gynes, and males) are described for M. camargoi, workers and gynes are described for M. erectapilosa, and only workers are described for M. bucki. Because the erect pilosity encountered in these species contradicts the state previously considered diagnostic for the genus, that of appressed, spatulate or squamiform pilosity found in all other Myrmicocrypta species, we necessarily discuss the characters that define the genus Myrmicocrypta and review its phylogenetic position within the tribe Attini.