Summary The scope of plant control over its microbiome is a central question in evolutionary biology and agriculture. Leaf traits are known to shape pathogen colonization and disease development, but their impact on the broader community of largely non‐pathogenic fungi that colonize plant leaves remains an open question. We used reciprocal common gardens of the model tree, Populus trichocarpa (black cottonwood), to examine relationships between leaf traits and the leaf mycobiome in two strongly contrasting environments. We measured six leaf traits (stomatal length, stomatal density, carbon‐to‐nitrogen ratio, leaf thickness, leaf dry matter content, and specific leaf area) and used fungal marker gene sequencing to characterize leaf fungal communities for 57 tree genotypes replicated in one mesic and one xeric common garden (809 trees). Several leaf traits covaried with the leaf mycobiome, yet one relationship was paramount: plant genotypes with longer, sparser leaf stomata hosted a greater richness and diversity of more similar fungal species compared to plant genotypes with shorter, denser leaf stomata. These relationships, while modulated by the environment plants were sourced from and grown in, suggest that stomatal traits may be a general mechanism through which plants and the leaf mycobiome influence one another.