Biotic communities typically include multiple species with similar resource requirements, and the mechanisms that promote such coexistence are a major focus of ecological inquiry. Here we present results of a multi-year study on the spatial and temporal patterns of habitation of a myrmecophytic tree, Cordia alliodora, by several species of ants. We examined whole-tree ant occupancy for three ages of C. alliodora, tested for within-tree microhabitat selection among ant occupants and studied the patterns of colonization of young plants and colony expansion on older plants. Although two ant species, Azteca pittieri and Crematogaster carinata, were clearly dominant overall, multiple factors related to the interactions among the ants, the host plant and other insects allowed subdominant species to persist. Specifically, we suggest that changes in the available habitat with plant ontogeny, differences among ant species in reliance upon homopteran honeydew, competition among ants for domatia, variation in the colonization ability of ant species, and parasitoid attack on the dominant species were primary mechanisms that resulted in the coexistence of multiple ant species at the individual plant and population levels. Our results reinforce the emerging consensus that studies on the evolution and ecology of ant-plant mutualisms benefit from a holistic approach incorporating the complex relationships among competitors, partners, and natural enemies rather than just pairwise interactions between focal ant and plant species.