Disturbance, productivity, and natural enemies are significant determinants of the evolution of diversity, but their interactive effect remains unresolved. We develop a simple, qualitative model assuming trade-offs between growth rate, competitive ability and parasite resistance, to address the interactive effects of these variables on the evolution of host diversity. Consistent with previous studies our model predicts maximum diversity at intermediate levels of disturbance and productivity in the absence of parasitism. However, parasites break down these unimodal diversity relationships with productivity and disturbance, as selection for parasite resistance reduces the importance of growth rate-competitive ability trade-offs. We tested these predictions using the bacterium Pseudomonas fluorescens, which undergoes an adaptive radiation into spatial niche specialists under laboratory conditions. This is the first study of adaptive radiation in response to experimental manipulation of the three-way interaction between productivity, disturbance, and natural enemies. As hypothesized, unimodal diversity relationships with disturbance and productivity were weakened or disappeared in the presence of parasitic phages. This was the result of phages increasing diversity at environmental extremes, by imposing selection for phage-resistant variants, but decreasing diversity in less stressful environments, probably through reductions in resource competition. Phages had a net effect of increasing host diversity. Parasites and other natural enemies are therefore likely to have a large effect in mitigating the influence of other environmental variables on the evolution and maintenance of diversity.