Acremonium is known to be regularly isolated from food and also to be a cause of human disease. Herein, we resolve some sources of confusion that have strongly hampered the accurate interpretation of these and other isolations. The recently designated type species of the genus Acremonium, A. alternatum, is known only from a single isolate, but it is the closest known relative of what may be one of the planet’s most successful organisms, Acremonium sclerotigenum/egyptianum, shown herein to be best called by its earliest valid name, A. egyptiacum. The sequencing of ribosomal internal transcribed spacer (ITS) regions, actin genes, or both for 72 study isolates within this group allowed the full range of morphotypes and ITS barcode types to be elucidated, along with information on temperature tolerance and habitat. The results showed that nomenclatural confusion and frequent misidentifications facilitated by morphotaxonomy, along with misidentified early sequence deposits, have obscured the reality that this species is, in many ways, the definitive match of the historical concept of Acremonium: a pale orange or dull greenish-coloured monophialidic hyphomycete, forming cylindrical, ellipsoidal, or obovoid conidia in sticky heads or obovoid conidia in dry chains, and acting ecologically as a soil organism, marine organism, plant pathogen, plant endophyte, probable insect pathogen, human opportunistic pathogen, food contaminant, probable dermatological communicable disease agent, and heat-tolerant spoilage organism. Industrially, it is already in exploratory use as a producer of the antibiotic ascofuranone, active against trypanosomes, cryptosporidia, and microsporidia, and additional applications are in development. The genus-level clarification of the phylogeny of A. egyptiacum shows other historic acremonia belong to separate genera, and two are here described, Parasarocladium for the Acremonium radiatum complex and Kiflimonium for the Acremonium curvulum complex.