Evolutionary innovations are often achieved by repurposing existing genes to perform new functions; however, the mechanisms enabling the transition from old to new remain controversial. We identified mutations in bacteriophage lambda's host-recognition gene J that confer enhanced adsorption to lambda's native receptor, LamB, and the ability to access a new receptor, OmpF. The mutations destabilize lambda particles and cause conformational bistability of J, which yields progeny of multiple phenotypic forms, each proficient at different receptors. This work provides an example of how nongenetic protein variation can catalyze an evolutionary innovation. We propose that cases where a single genotype canmanifest asmultiple phenotypes may bemore common than previously expected and offer a generalmechanism for evolutionary innovation.