Arbuscular mycorrhizal fungi (AMF) are ubiquitous in cultivated soils, forming symbiotic relationships with the roots of major crop species. Studies in controlled conditions have demonstrated the potential of AMF to enhance the growth of host plants. However, it is difficult to estimate the actual benefit in the field, not least because of the lack of suitable AMF-free controls. Here we implement a novel strategy using the selective incorporation of AMF-resistance into a genetic mapping population to evaluate maize response to AMF. We found AMF to account for about one-third of the grain production in a medium input field, as well as to affect the relative performance of different plant genotypes. Characterization of the genetic architecture of the host response indicated a trade-off between mycorrhizal dependence and benefit. We identified several QTL linked to host benefit, supporting the feasibility of breeding crops to maximize profit from symbiosis with AMF.