Bacteria encode diverse genetic systems that enable them to fight against phage predation. While several of these systems have been thoroughly characterised (such as CRISPR-Cas and Restriction Modification), the molecular mechanism of many remains unknown. Here we study the uncharacterised anti-phage system Kiwa, composed of two proteins, KwaA containing transmembrane domains, and KwaB encoding a domain of unknown function. We studied Kiwa by collecting all Kiwa operons present in the NCBI database and performing a phylogenetic analysis that resulted in distinct clades for both KwaA and KwaB genes. Interestingly, KwaB homologs all contained a DUF4868 domain, whilst KwaA homologs showed diversity in size and number of encoded transmembrane regions (TM-region). We therefore selected Kiwa operons present in different clades to test for anti-phage activity. We found that Kiwa systems can give up to 105-fold protection against specific phage families, with anti-phage activity being lost upon deletion of KwaA or KwaB, and truncation of KwaA. Interestingly, the presence of four TM-regions in KwaA is essential for protection, as reconstitution of four regions in Kiwa operons of two TM-regions resulted in anti-phage activity not previously observed. Phage escape mutants revealed that Kiwa is activated when KwA detects the inhibition of the host RNA polymerase by a phage-encoded protein. This activation triggers the activation of KwaB, which forms oligomers and, through an unidentified process, initiates the degradation of phage DNA via RecBCD. Remarkable, this degradation occurs even when the phage produces RecBCD inhibitors, effectively preventing the spread of progeny within the cell population.