We studied the morphology, morphometry, resting cysts, and molecular phylogeny of a new woodruffiid ciliate, Etoschophrya inornata, from ephemeral puddles and two lacustrine habitats in Idaho, Northwest U.S.A. Up to now the genus Etoschophrya has included a single species, E. oscillatoriophaga, from which our new form is distinguished by (1) the absence of interkinetal cortical granules and, consequently, the absence of extrusible red material in methyl green-pyronin stains; (2) usually ≥ five adoral membranelles vs. usually four; (3) greater length and length:width ratio; (4) prominent cortical furrows vs. inconspicuous; and (5) adaptation to nonsaline semiterrestrial and lacustrine habitats in the Nearctic vs. highly saline alkaline Afrotropic soil habitats. Resting cysts have two distinct membranes and a thick hyaline mucous pericyst layer. However, only one membrane persists in older cysts. Like its congener, E. inornata feeds exclusively on filamentous cyanobacteria. The 18S rRNA gene sequence places this species in a strongly supported clade with Kuklikophrya ougandae basal to the other platyophryids. We include a morphologic cladistic analysis of platyophryid ciliates and present a hypothetical scenario for the evolution of the platyophryid oral structures.