Complex and interacting selective pressures can produce bacterial communities with a range of phenotypes. One measure of bacterial success is the ability of cells or populations to proliferate while avoiding lytic phage infection. Resistance against bacteriophage infection can occur in the form of a metabolically expensive exopolysaccharide capsule. Here, we show that in Caulobacter crescentus, presence of an exopolysaccharide capsule provides measurable protection against infection from a lytic paracrystalline S-layer bacteriophage (CR30), but at a metabolic cost that reduces success in a phage-free environment. Carbon flux through GDP-mannose 4,6 dehydratase in different catabolic and anabolic pathways appears to mediate this trade-off. Together, our data support a model in which diversity in bacterial communities may be maintained through variable selection on phenotypes utilizing the same metabolic pathway.