Pseudomonas aeruginosa is an opportunistic bacterial pathogen. Most P. aeruginosa isolates are infected by a filamentous virus (phage) called Pf. At sites of infection, filamentous Pf virions accumulate where they increase mucus viscosity, promote bacterial colonization, and directly stimulate innate anti-viral immune responses that inhibit bacterial clearance. Entropic interactions between Pf virions and non-adsorbing biological polymers such as DNA, hyaluronan, mucin, etc. cause filamentous Pf virions to assemble into a liquid crystalline structure that protects bacteria from antibiotics. Additionally, Pf phages encode proteins that modulate the secretion of bacterial virulence factors such as the green pigment pyocyanin. Animal immune systems use conserved AhR receptors to detect bacterial pigments to monitor bacterial burden at sites of infection. We used genetics and quantitative proteomics to discover that Pf phage inhibit PQS quorum sensing to reduce pyocyanin production, allowing P. aeruginosa to evade AhR-mediated immune responses. Despite their simple morphology and small genome size (~10 kb), filamentous Pf phages participate in complex phage-host-microbe interactions that enhance pathogen fitness and influence infection outcomes.