Evolutionary game theory, specifically the game known as Prisoner’s Dilemma, can help explain how cheaters can invade populations despite being less reproductively fit than cooperators. Most strains of Pseudomonas aeruginosa contain Pf bacteriophages integrated in their genomes, and these filamentous phages can propagate without lysing their host. Pf phage infection is typically not costly and some benefits to P. aeruginosa have been described, including increased antimicrobial resistance. However, cell death may result when multiple Pf phages attack a cell or when Pf replication is uncontrolled. We observed extremely high levels of Pf5 phage replication when P. aeruginosa PA14 was experimentally evolved in media simulating nutrients from the cystic fibrosis airway. This Pf5 spread was caused by a mutated repressor gene (pf5r) within the prophage, which imposes significant costs on the host bacterium by reducing growth rate and total yield. Despite their lower absolute fitness relative to their ancestor strain, these bacteria containing hyperactive prophage could outcompete the ancestor in direct competition. These pf5r mutants are cheaters as releasing phage in the environment selfishly increases their own fitness at the cost of other competitors. It is unsurprising that viruses act selfishly, but more remarkable is that these mutant phage shift competitions between bacterial genotypes to prisoner’s dilemma, in which all genotypes evolve lower fitness as the pf5r mutation sweeps across the population. This study demonstrates that relationships between bacteria and prophage are unstable and can quickly remodel evolving microbial communities, including potentially during chronic infections caused by P. aeruginosa.