Many positive-stranded RNA viruses contain short, single-stranded 3' ends that are vulnerable to degradation by host cellular RNases. Therefore, the existence of a 3'-end repair mechanism (analogous to cellular telomerases) must be required and/or advantageous for RNA viruses. Accordingly, we provide evidence suggesting that deletions of up to 6 nt from the 3' end of satellite (sat-) RNA C (a small parasitic RNA associated with turnip crinkle carmovirus) are repaired to the wild-type sequence in vivo and in vitro. The novel 3'-end repair mechanism involves the production of 4-8 nt oligoribonucleotides by abortive synthesis by the viral replicase using the 3' end of the viral genomic RNA as template. Based on our in vitro results, we postulate that the oligoribonucleotides are able to prime synthesis of wild-type negative-strand sat-RNA C in a reaction that does not require base pairing of the oligoribonucleotides to the mutant, positive-strand RNA template. The discovery of a 3'-end repair mechanism opens up new strategies for interfering with viral infections.