In North America, Fusarium head blight is caused predominantly by Fusarium graminearum, a member of the F. sambucinum species complex (FSAMSC). However, recent largescale surveys revealed that other species in the FSAMSC and the F. tricinctum species complex (FTSC) have emerged as pathogens of wheat and barley in some settings. Among toxins produced by the FSAMSC, trichothecenes pose the most significant threat to public health. However, some fusaria in the FTSC can produce other mycotoxins, including enniatins (ENNs) and moniliformin (MON) which are also concern with respect to food and feed safety. Herein we conducted large surveys of FSAMSC and FTSC strains hosted in culture collections to evaluate their species diversity, mycotoxin potential, and pathogenicity towards wheat. Maximum likelihood (ML) analyses of a multilocus dataset revealed that the FSAMSC encompasses indeed 74 genealogically exclusive species, including 33 novel, distributed among six strongly supported clades: Sporotrichioides, Graminearum, Novel, Sambucinum, Longipes, and Brachygibbosum. Members of these clades produced type A, type B, or both types of trichothecenes. Surprisingly, two novel species within the Sambucinum Clade synthesized two new type A trichothecenes, 15-keto NX-2 and 15-keto NX-3. These two species, with all members of the Graminearum Clade, were aggressive toward heads of the susceptible cultivar Apogee. Other taxa within the FSAMSC were nonpathogenic or infected only the inoculated floret. Altogether, these data highlight that aggressiveness toward wheat appears to be toxin–dependent and that it is not limited to F. graminearum and its close relatives. We also elucidate that the phylogenetic, mycotoxigenic, and pathogenic diversity of the FSAMSC and FTSC was underestimated, and their members uniformly produce several emerging and neglected mycotoxins. Evolutionary relationships inferred from a 5-locus sequence dataset resolved FTSC strains into 24 genealogically phylogenetically distinct species, of which nine were novel. Nineteen of the species were toxin-producing lineages that shared the same mycotoxin profile characterized by a production of ENNs, MON, aurofusarin (AUR), and 2-amino-14,16-dimethyloctadecan-3-ol (AOD). Interestingly, five species in the most basal clade of the FTSC phylogeny synthesized ENNs and/or AUR but did not produce MON or AOD.