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1. Microbial ecologists are intensely interested in the processes governing microbial community assembly; however, progress has been limited by a lack of studies that span multiple geographical scales and levels of biological organization.

2. We used high throughput sequencing to characterize foliar fungal endophyte communities and host plant genetic structure both within and among 24 populations of spotted locoweed Astragalus lentiginosus across the Great Basin Desert.

3. Across the Great Basin, both within and among populations of the host plant, fungal endophyte richness was predicted by plant size and variation in the seed-borne, heritable fungus, Alternaria fulva, which produces the bioactive alkaloid swainsonine.

4. The degree of between-plant turnover in the endophyte community was inversely related to host plant inbreeding and average plant size and positively related to the relative abundance of A. fulva. Plant size was inversely related to endophyte community richness, both among and within populations. The genetic and physical distance between host populations was not predictive of differences in fungal community structure.

5. Synthesis. Through pairing intensive local and regional sampling, we uncovered a primacy of deterministic forces imposed by a heritable symbiont on the community structure of locoweed endophytes.