The CRISPR-Cas system is a prokaryotic immune mechanism that protects against viral and other genome invaders. This system involves small RNAs (psiRNAs) derived from CRISPR loci and Cas proteins, particularly the RAMP module (Cmr) proteins. The study identifies a psiRNA-Cmr protein complex that cleaves complementary target RNAs at a fixed distance from the 3' end of the psiRNAs. In *Pyrococcus furiosus*, psiRNAs occur in two size forms with distinct 3' ends that direct cleavage at two sites on the target RNA. The psiRNA-Cmr complex is purified and characterized, and its function is demonstrated through cleavage assays. The results indicate that the psiRNA-Cmr complex functions as a homology-dependent RNA cleavage machinery, with each psiRNA species guiding cleavage at a specific site. The mechanism involves a 14-nucleotide counting mechanism anchored by the 3' end of the psiRNA, and the complex requires five of the six Cmr proteins for activity. The findings provide insights into the RNA silencing pathway in prokaryotes and highlight the diversity of CRISPR-Cas systems across different organisms.The CRISPR-Cas system is a prokaryotic immune mechanism that protects against viral and other genome invaders. This system involves small RNAs (psiRNAs) derived from CRISPR loci and Cas proteins, particularly the RAMP module (Cmr) proteins. The study identifies a psiRNA-Cmr protein complex that cleaves complementary target RNAs at a fixed distance from the 3' end of the psiRNAs. In *Pyrococcus furiosus*, psiRNAs occur in two size forms with distinct 3' ends that direct cleavage at two sites on the target RNA. The psiRNA-Cmr complex is purified and characterized, and its function is demonstrated through cleavage assays. The results indicate that the psiRNA-Cmr complex functions as a homology-dependent RNA cleavage machinery, with each psiRNA species guiding cleavage at a specific site. The mechanism involves a 14-nucleotide counting mechanism anchored by the 3' end of the psiRNA, and the complex requires five of the six Cmr proteins for activity. The findings provide insights into the RNA silencing pathway in prokaryotes and highlight the diversity of CRISPR-Cas systems across different organisms.