AbstractThe Diphyllatea (CRuMs) are heterotrophic protists currently divided into three distinct clades (Diphy I–III). Diphy I are biflagellates in the genus Diphylleia, whereas Diphy II and III represent cryptic clades comprising Collodictyon‐type quadriflagellates that were recently distinguished based on rRNA gene phylogenies. Here, we isolated Diphyllatea from freshwater crater lakes on two South Pacific islands and generated high‐quality transcriptomes from species representing each clade, including the first transcriptomic data from Diphy III. Phylogenomic analyses support the separation of Diphy II and III, while transcriptome completeness highlights the utility of these data for future studies. Lastly, we discuss the biogeography and ecology of Diphyllatea on these remote islands.