The study identifies a novel pathway for CRISPR RNA maturation in *Streptococcus pyogenes*, involving a trans-encoded small RNA (tracrRNA) and host factors RNase III and Csn1. TracrRNA, transcribed from the opposite strand of the CRISPR locus, base-pairs with pre-crRNA, leading to their co-processing and subsequent cleavage by RNase III. This process is essential for the production of active crRNAs and the protection of *S. pyogenes* against lysogenic phages. The study also reveals that tracrRNA-mediated crRNA maturation is conserved in other bacterial species with type II CRISPR/Cas systems, suggesting a widespread mechanism for RNA maturation in these systems.The study identifies a novel pathway for CRISPR RNA maturation in *Streptococcus pyogenes*, involving a trans-encoded small RNA (tracrRNA) and host factors RNase III and Csn1. TracrRNA, transcribed from the opposite strand of the CRISPR locus, base-pairs with pre-crRNA, leading to their co-processing and subsequent cleavage by RNase III. This process is essential for the production of active crRNAs and the protection of *S. pyogenes* against lysogenic phages. The study also reveals that tracrRNA-mediated crRNA maturation is conserved in other bacterial species with type II CRISPR/Cas systems, suggesting a widespread mechanism for RNA maturation in these systems.