Eucomonympha imla is a hypermastigote parabasalian found in the gut of the wood-feeding cockroach Cryptocercus punctulatus. It has received little attention since its original description in 1934 as the type species of the genus Eucomonympha and the family Eucomonymphidae. We used light and scanning electron microscopy to characterize surface morphology and organelles, with particular attention to the form of the rostrum, operculum, nucleus, and parabasals. Two previously unrecognized groups of bacterial ectobionts were observed-spirochetes that associate with the flagella and one or more types of rod-shaped bacteria that adhere to the cell surface. The small subunit rRNA (SSU rRNA) sequence was determined from manually isolated cells, and phylogenetic analyses place E. imla in a strongly supported clade with the genera Teranympha and Pseudotrichonympha and three sequences from formally undescribed termite symbionts provisionally assigned to Eucomonympha. Unexpectedly, the Eucomonympha isolates from termites are more closely related to Teranympha than to the type species, suggesting these should not be classified as species of Eucomonympha, despite their morphological similarity to E. imla. Eucomonymphidae fall within a strongly supported Trichonymphida (also including Hoplonymphidae, Trichonymphidae, and Staurojoeninidae), but this clade branches separately from other hypermastigote groups (lophomonads and spirotrichonymphids), suggesting that hypermastigotes are polyphyletic.