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The genus Ceratocystis was established in 1890 and accommodates many important fungi. These include serious plant pathogens, significant insect symbionts and agents of timber degradation that result in substantial economic losses. Virtually since its type was described from sweet potatoes, the taxonomy of Ceratocystis has been confused and vigorously debated. In recent years, particulary during the last two decades, it has become very obvious that this genus includes a wide diversity of very different fungi. These have been roughly lumped together due to their similar morphological structures that have clearly evolved through convergent evolution linked to an insect-associated ecology. As has been true for many other groups of fungi, the emergence of DNA-based sequence data and associated phylogenetic inferences, have made it possible to robustly support very distinct boundaries defined by morphological characters and ecological differences. In this study, DNA-sequence data for three carefully selected gene regions (60S, LSU, MCM7) were generated for 79 species residing in the aggregate genus Ceratocystis sensu lato and these data were subjected to rigorous phylogenetic analyses. The results made it possible to distinguish seven major groups for which generic names have been chosen and descriptions either provided or emended. The emended genera included Ceratocystis sensu stricto, Chalaropsis, Endoconidiophora, Thielaviopsis, and Ambrosiella, while two new genera, Davidsoniella and Huntiella, were described. In total, 30 new combinations have been made. This major revision of the generic boundaries in the Ceratocystidaceae will simplify future treatments and work with an important group of fungi including distantly related species illogically aggregated under a single name.