Temperate phages engage in long-term associations with their hosts that may lead to mutually beneficial interactions, of which the full extent is presently unknown. Here, we describe an environmentally relevant model system with a single host, a species of the Roseobacter clade of marine bacteria, and two genetically similar phages (ɸ-A and ɸ-D). Superinfection of a ɸ-D lysogenized strain (CB-D) with ɸ-A particles resulted in a lytic infection, prophage induction, and conversion of a subset of the host population, leading to isolation of a newly ɸ-A lysogenized strain (CB-A). Phenotypic differences, predicted to result from divergent lysogenic-lytic switch mechanisms, are evident between these lysogens, with CB-A displaying a higher incidence of spontaneous induction. Doubling times of CB-D and CB-A in liquid culture are 75 and 100 min, respectively. As cell cultures enter stationary phase, CB-A viable counts are half of CB-D. Consistent with prior evidence that cell lysis enhances biofilm formation, CB-A produces twice as much biofilm biomass as CB-D. As strains are susceptible to infection by the opposing phage type, co-culture competitions were performed to test fitness effects. When grown planktonically, CB-A outcompeted CB-D three to one. Yet, during biofilm growth, CB-D outcompeted CB-A three to one. These results suggest that genetically similar phages can have divergent influence on the competitiveness of their shared hosts in distinct environmental niches, possibly due to a complex form of phage-mediated allelopathy. These findings have implications for enhanced understanding of the eco-evolutionary dynamics of host-phage interactions that are pervasive in all ecosystems.