Bacteriophage are numerically the most abundant organisms on the planet and it is therefore not surprising that they play significant roles in the ecology of bacteria. The best understood mechanisms by which phage affect microorganisms is through their lytic activity. In this capacity, phage play an important role in nutrient cycling as well as in modulation of microbial abundance. What is less well understood is the role of filamentous phage, which do not normally lyse their host cell during the replication cycle. In this study, we have focused on the role of a Pseudomonas aeruginosa filamentous prophage, Pf4, in mediating stress resistance, virulence and biofilm formation. The phage also plays a role in self-competition during mono-species but not during mixed species biofilm development. Our results clearly show that the phage plays an important role in biofilm development, resistance to surfactant stress, the generation of genetic variants as well as virulence in a mouse model of lung infection. We further show that these phenotypes are linked to conversion of the phage into a superinfective form that can induce host cell lysis. Further work links the development of superinfection to reactive oxygen-induced mutations in a single genetic locus in the phage. This locus, repC, has homology to immunity proteins from other bacteriophage. Using a combination of genetic deletions and complementation as well as RNA and ChIPseq, we show that the Pf4 encoded RepC can bind to and regulate the expression of not only the Pf4 encoded genes, but virulence factor and stress associated genes in the P. aeruginosagenome. We have also generated crystal structures of the RepC gene to model how it binds to consensus sequences. These data show that the Pf4 phage, plays an important role in regulating host gene expression and may explain why filamentous phage are not eliminated by their host. These data also further blur the lines between host and parasite.