Phylogenetic relationships among the hymenomycetous yeasts in the Cryptococcus luteolus lineage of the Tremellales were examined based on sequence analyses of the 18S rRNA gene, 26S rRNA gene D1/D2 domain, internal transcribed spacer (ITS) region including 5.8S rRNA gene and mitochondrial cytochrome b gene. In addition to the Dioszegia clade, two clades represented by Bullera mrakii and Bullera sinensis, respectively, were revealed to be well‐separated monophyletic groups in the lineage. These clades also exhibited distinguishable colony characters. Two new genera, Derxomyces gen. nov. (type species: Derxomyces mrakii comb. nov.) and Hannaella gen. nov. (type species: Hannaella sinensis comb. nov.), are proposed to accommodate the species in the B. mrakii and B. sinensis clades, respectively. Mainly based on D1/D2 and ITS sequence comparison, eight novel Derxomyces species were recognized from ballistoconidium‐forming strains isolated from plant leaves. The new species and their type strains are as follows: Derxomyces boekhoutii (AS 2.3758T=CBS 10824T), Derxomyces hainanensis (AS 2.3467T=CBS 10820T), Derxomyces linzhiensis (AS 2.2668T=CBS 10827T), Derxomyces pseudocylindrica (AS 2.3778T=CBS 10826T), Derxomyces qinlingensis (AS 2.2446T=CBS 10818T), Derxomyces simaoensis (AS 2.3571T=CBS 10822T), Derxomyces wuzhishanensis (AS 2.3760T=CBS 10825T) and Derxomyces yunnanensis (AS 2.3562T=CBS 10821T).