Bacteria have evolved multiple defense systems, including CRISPR-Cas, to cleave the DNA of phage and mobile genetic elements (MGE). In turn, phages have evolved anti-CRISPR (Acr) proteins that use novel and co-opted mechanisms to block DNA binding or cleavage. We previously found that an anti-CRISPR protein (AcrVA2) unexpectedly inhibits Cas12a biogenesis by binding conserved and functionally important amino acids in the Cas12a N-terminal polypeptide and degrading it. However, the mechanism of underlying Cas12a mRNA destruction remains mysterious. Here, we show that co-expressing AcrVA2 and Cas12a in a simplified invitro transcription-translation assay does not trigger Cas12a mRNA degradation, indicating that other bacterial factors are required. Inhibition of Rho terminase, which mediates premature transcriptional termination, does not affect Cas12a mRNA downregulation, suggesting that Rho is not involved. We then tested the role of transfer-messenger  RNA (tmRNA), which rescues ribosomes stalled during translation and triggers degradation of the truncated mRNA and polypeptide via trans-translation. Deletion of tmRNA restores fragments of Cas12a mRNA, indicating a role in Cas12a downregulation. Continuous co-expression of AcrVA2 recruits mysterious host factors to truncate Cas12a mRNA during translation and then targets the truncated Cas12a mRNA and protein for destruction via trans-translation.