Experimental tests of community assembly mechanisms for host-associated microbiomes in nature are lacking. Asymptomatic foliar fungal endophytes are a major component of the plant microbiome and are increasingly recognized for their impacts on plant performance, including pathogen defense, hormonal manipulation, and drought tolerance. However, it remains unclear whether fungal endophytes preferentially colonize certain host ecotypes or genotypes, reflecting some degree of biotic adaptation in the symbioses, or whether colonization is simply a function of spore type and abundance within the local environment. Whether host ecotype, local environment, or some combination of both controls the pattern of microbiome formation across hosts represents a new dimension to the age-old debate of nature versus nurture. Here, we used a reciprocal transplant design to explore the extent of host specificity and biotic adaptation in the plant microbiome, as evidenced by differential colonization of host genetic types by endophytes. Specifically, replicate plants from three locally-adapted ecotypes of the native grass Panicum virgatum (switchgrass) were transplanted at three geographically distinct field sites (one home and two away) in the Midwestern US. At the end of the growing season, plant leaves were harvested and the fungal microbiome characterized using culture-dependent sequencing techniques. Our results demonstrated that fungal endophyte community structure was determined by local environment (i.e., site), but not by host ecotype. Fungal richness and diversity also strongly differed by site, with lower fungal diversity at a riparian field site, whereas host ecotype had no effect. By contrast, there were significant differences in plant phenotypes across all ecotypes and sites, indicating ecotypic differentiation of host phenotype. Overall, our results indicate that environmental factors are the primary drivers of community structure in the switchgrass fungal microbiome.