Plant genetic and ontogenetic variation can significantly impact dependent fungal and arthropod communities. However, little is known of the relative importance of these extended genetic and ontogenetic effects within a species. Using a common garden trial, we compared the dependent arthropod and fungal community on 222 progeny from two highly differentiated populations of the endangered heteroblastic tree species, Eucalyptus morrisbyi. We assessed arthropod and fungal communities on both juvenile and adult foliage. The community variation was related to previous levels of marsupial browsing, as well as the variation in the physicochemical properties of leaves using near-infrared spectroscopy. We found highly significant differences in community composition, abundance and diversity parameters between eucalypt source populations in the common garden, and these were comparable to differences between the distinctive juvenile and adult foliage. The physicochemical properties assessed accounted for a significant percentage of the community variation but did not explain fully the community differences between populations and foliage types. Similarly, while differences in population susceptibility to a major marsupial herbivore may result in diffuse genetic effects on the dependent community, this still did not account for the large genetic-based differences in dependent communities between populations. Our results emphasize the importance of maintaining the populations of this rare species as separate management units, as not only are the populations highly genetically structured, this variation may alter the trajectory of biotic colonization of conservation plantings.