The ribosome can change its reading frame during translation in a process known as programmed ribosomal frameshifting. These rare events are supported by complex mRNA signals. However, we found that the ciliates Euplotes crassus and Euplotes focardii exhibit widespread frameshifting at stop codons. 47 different codons preceding stop signals resulted in either +1 or +2 frameshifts, with the +1 frameshifting at AAA being the most frequent. The frameshifts show unusual plasticity and rapid evolution, and have little influence on translation rates. Proximity of a stop codon to the 3′-mRNA end rather than its occurrence or sequence context appeared to designate termination. Thus, a stop codon is not a sufficient signal for translation termination, and the default function of stop codons in Euplotes is frameshifting, whereas termination is specific to certain mRNA positions and likely requires additional factors