Many bacteria contain an ortholog of the Ro autoantigen, a ring-shaped protein that binds noncoding RNAs (ncRNAs) called Y RNAs. In the only studied bacterium, Deinococcus radiodurans, the Ro ortholog Rsr functions in heat-stress-induced ribosomal RNA (rRNA) maturation and starvation-induced rRNA decay. However, the mechanism by which this conserved protein and its associated ncRNAs act has been obscure. We report that Rsr and the exoribonuclease polynucleotide phosphorylase (PNPase) form an RNA degradation machine that is scaffolded by Y RNA. Single-particle electron microscopy, followed by docking of atomic models into the reconstruction, suggests that Rsr channels single-stranded RNA into the PNPase cavity. Biochemical assays reveal that Rsr and Y RNA adapt PNPase for effective degradation of structured RNAs. A Ro ortholog and ncRNA also associate with PNPase in Salmonella Typhimurium. Our studies identify another ribonucleoprotein machine and demonstrate that ncRNA, by tethering a protein cofactor, can alter the substrate specificity of an enzyme. Display omitted ► A bacterial Ro protein is complexed with ncRNA and the PNPase exoribonuclease ► ncRNA scaffolds this RNA degradation machine ► Single-particle EM suggests that Rsr channels RNA into the PNPase cavity ► Rsr and the ncRNA specialize PNPase for degrading structured RNA A bacterial Y noncoding RNA is found to tether Ro protein to polynucleotide phosphorylase exoribonuclease, specializing this enzyme for degrading structured RNAs. Thus, a noncoding RNA can alter the substrate specificity of an enzyme by tethering a protein cofactor.