The nature and stability of coexistence of specialist species with more generalized competitors present theoretical questions that have been difficult to resolve. Recent surveys of bacteriophage host-ranges suggest that generalist phage often coexistent with specialists. However, previous theoretical work has explained this coexistence only in terms of strict genetic trade-offs, which are not consistently observed when phage are challenged to evolve to multiple hosts in laboratory environments. Here we use the framework of optimal foraging to identify conditions that might prevent generalists from outcompeting specialist relatives. Our analysis shows that heterogeneities in phage life-history properties make host-range specialist more viable, and that endogenous fluctuations in host density permit a narrow window of stable coexistence between specialists and generalists without the need for genetic trade-offs. These results are especially relevant for understanding the barriers to the evolution of broader host-ranges in bacteriophage and other pathogens with similar life-cycles.