Parabasalia represents a complex assemblage of species, which recently received extensive reorganization. The newly created order Cristamonadida unites complex hypermastigids belonging to the Lophomonadida like the joeniids, the multinucleate polymonad Calonymphidae, and well-developed trichomonads in the Devescovinidae. All these protists exclusively occur in the guts of termites and related insects. In this study, small subunit rRNA and glyceraldehyde-3-phosphate dehydrogenase genes were identified without cultivation from 14 species in Cristamonadida including previously unstudied genera such as Joenina, Joenia, Joenoides, Macrotrichomonas, Gigantomonas, and Foaina. Despite the great morphological diversity of Cristamonadida, our phylogenetic analyses supported the monophyly of this order. However, almost all the families and subfamilies composing this order are polyphyletic suggesting a complicated morphological evolution. Our analyses also showed that Cristamonadida descends from one lineage of rudimentary trichomonads and that joeniids was basal in this order. Several successive and independent morphological transitions such as the development and reduction of flagellar apparatus and associated cytoskeleton and transition to multinucleated status have likely led to the diversity and complexity of cristamonad lineages.