The fungal genus Conidiobolus sensu lato was delimited into four genera based on morphology and phylogeny. However, the taxonomic placement of C. parvus has not been determined until now. Here, we show that C. parvus belongs to a distinct lineage based on mitochondrial (mtSSU) and nuclear (TEF1 and nrLSU) phylogenetic analyses. Phylogenetic analyses further revealed a new species as sister to C. parvus. We identified a synapomorphy uniting these lineages (azygospore production) that was not observed in other allied genera of the family Ancylistaceae, and erected a new genus Azygosporusgen. nov. for this monophyletic group, with a new combination, A. parvuscomb. nov. as the type species. Within Azygosporus, the novel species A. macropapillatussp. nov. was introduced from China based on morphological characteristics and molecular evidence, which is characterized by its prominent basal papilla, in comparison to other closely related species, measuring 7.5–10.0×5.0–10.0 µm. Our study resolved the phylogenetic placement of C. parvus and improved the taxonomic system of the Ancylistaceae family.