A major goal of community genetics is to understand the influence of genetic variation within a species on ecological communities. Although well-documented for some organisms, additional research is necessary to understand the relative and interactive effects of genotype and environment on biodiversity, identify mechanisms through which tree genotype influences communities, and connect this emerging field with existing themes in ecology. We employ an underutilized but ecologically significant group of organisms, epiphytic bark lichens, to understand the relative importance of Populus angustifolia (narrowleaf cottonwood) genotype and environment on associated organisms within the context of community assembly and host ontogeny. Several key findings emerged. (1) In a single common garden, tree genotype explained 18–33% and 51% of the variation in lichen community variables and rough bark cover, respectively. (2) Across replicated common gardens, tree genotype affected lichen species richness, total lichen cover, lichen species composition, and rough bark cover, whereas environment only influenced composition and there were no genotype by environment interactions. (3) Rough bark cover was positively correlated with total lichen cover and richness, and was associated with a shift in species composition; these patterns occurred with variation in rough bark cover among tree genotypes of the same age in common gardens and with increasing rough bark cover along a ~40 year tree age gradient in a natural riparian stand. (4) In a common garden, 20-year-old parent trees with smooth bark had poorly developed lichen communities, similar to their 10-year-old ramets (root suckers) growing in close proximity, while parent trees with high rough bark cover had more developed communities than their ramets. These findings indicate that epiphytic lichens are influenced by host genotype, an effect that is robust across divergent environments. Furthermore, the response to tree genotype is likely the result of genetic variation in the timing of the ontogenetic shift from smooth to rough bark allowing communities on some genotypes to assemble faster than those on other genotypes. Organisms outside the typical sphere of community genetics, such as lichens, can help address critical issues and connect plant genotype effects to long-established streams of biological research, such as ontogeny and community assembly.