Deviant genetic codes reported in ciliates share the same feature: one (UGA) or two (UAR) of the three canonical stop codons are translated into one particular amino acid. In many genera, such as Oxytricha, Paramecium, and Tetrahymena, UAR codons are translated into glutamine. UGA is translated into cysteine in Euplotes or into tryptophan in Colpoda inflata and Blepharisma americanum. Here, we show that three peritrich species (Vorticella microstoma, Opisthonecta henneguyi, and Opisthonecta matiensis) translate UAA into glutamate and that at least UAA in O. matiensis is decoded through a mutant suppressor-like tRNA. This kind of genetic code has never been reported for any living organism. Phylogenetic analysis with alpha-tubulin sequences corroborates that peritrichs, peniculines (Paramecium), and hymenostomates (Tetrahymena) form a monophyletic group (class Oligohymenophorea). The differential translation (glu/gln) of UAR codons, the monophyly of the Oligohymenophorea, and the common evolutionary origin of glutamate and glutamine suggest that deviant genetic codes of present-day oligohymenophoreans could have the same origin.