A key problem in evolutionary biology is to understand how multispecific networks are reshaped by evolutionary and coevolutionary processes as they spread across contrasting environments. To address this problem, we need studies that explicitly evaluate the multispecific guild structure of coevolutionary processes and some of their key outcomes such as local adaptation. We evaluated geographic variation in interactions between most extant native populations of Monterey pine (Pinus radiata) and the associated resistant-propagule community (RPC) of ectomycorrhizal (EM) fungi, using a reciprocal cross-inoculation experiment with all factorial combinations of plant genotypes and soils with fungal guilds from each population. Our results suggest that the pine populations have diverged in community composition of their RPC fungi, and have also diverged genetically in several traits related to interactions of seedlings with particular EM fungi, growth, and biomass allocation. Patterns of genetic variation among pine populations for compatibility with EM fungi differed for the three dominant species of EM fungi, suggesting that Monterey pines can evolve differently in their compatibility with different symbiont species.