Rapid evolution contributes to frequent emergence of RNA viral pathogens on novel hosts. However, accurately predicting which viral genotypes will emerge has been elusive. Prior work with lytic RNA bacteriophage ɸ6 (family Cystoviridae) suggested that evolution under low multiplicity of infection (MOI; proportion of viruses to susceptible cells) selected for greater host exploitation, while evolution under high MOI selected for better intracellular competition against co-infecting viruses. We predicted that phage genotypes that had experienced 300 generations of low MOI ecological history would be relatively advantaged in initial growth on two novel hosts. We inferred viral growth through changes in host population density, specifically by analyzing five attributes of growth curves of infected bacteria. Despite equivalent growth of evolved viruses on the original host, low MOI evolved clones were generally advantaged relative to high MOI clones in exploiting novel hosts. However, the specific attributes of growth curves that supported their advantage differed by host, indicating interactions between both viral and host genotype. Although there will be host specificity in viral growth, we suggest based on infectivity differences of viruses from high versus low MOI histories that prior MOI selection can later affect emergence potential.