Vibrio cholerae is a major human pathogen that causes the diarrheal disease cholera. A crucial aspect in the pathogenesis of the disease is cell-cell communication, a.k.a quorum sensing (QS), which coordinates community behaviours such as biofilm formation and toxin production. The cholera toxin is encoded by the filamentous bacteriophage CTXϕ which is irreversibly integrated into the host chromosome. Lysogenic induction of CTXϕ is well studied at the transcriptional level and depends on the host-encoded SOS response regulator LexA and the phage-encoded repressor RstR. However, post-transcriptional regulation of CTXϕ has not been studied and identifying potential post-transcriptional regulators of CTXϕ is challenging as it is only poorly expressed under standard laboratory conditions. To address this question, we performed transcriptomic analysis of V. cholerae under virulence-inducing conditions, resulting in the identification of dozens of differentially expressed sRNAs, including the well-characterized TarB and CarZ sRNAs, as well as several uncharacterized sRNAs. To investigate the global RNA-RNA network under virulence conditions, we used RIL-seq (RNA-interaction-by-ligation-and-sequencing). Our analysis captured 1,395 RNA-RNA chimeras interacting with Hfq, including a novel virulence-related sRNA that we named CisR (CTX inhibiting small RNA). We discovered that CisR base-pairs with and inhibits the expression of the cep mRNA, encoding a core structural element of the CTXϕ phage, and that the CisR sRNA is processed by RNAse E from the 3"UTR of the prtV mRNA, which encodes an M6 metalloprotease that is relevant for invasion of the mammalian host. Further, we found that two global regulators activate cisR transcription: the quorum-sensing regulator HapR in a cell density dependent manner, and the cyclic AMP receptor protein (CRP) in response to carbon starvation. Taken together, our data indicate that the core-genome encoded CisR sRNA controls the production of the horizontally acquired virulence gene that has a crucial role in the life cycle of the CTXϕ phage.