Despite the ubiquity and importance of microbes in nature, little is known about their natural population dynamics, especially for those that occupy terrestrial habitats. Here we investigate the dynamics of the yeast-like fungus Aureobasidium pullulans (Ap) on apple leaves in an orchard. We asked three questions. (1) Is variation in fungal population density among leaves caused by variation in leaf carrying capacities and strong density-dependent population growth that maintains densities near carrying capacity? (2) Do resident populations have competitive advantages over immigrant cells? (3) Do Ap dynamics differ at different times during the growing season? To address these questions, we performed two experiments at different times in the growing season. Both experiments used a 2 x 2 factorial design: treatment 1 removed fungal cells from leaves to reveal density-dependent population growth, and treatment 2 inoculated leaves with an Ap strain engineered to express green fluorescent protein (GFP), which made it possible to track the fate of immigrant cells. The experiments showed that natural populations of Ap vary greatly in density due to sustained differences in carrying capacities among leaves. The maintenance of populations close to carrying capacities indicates strong density-dependent processes. Furthermore, resident populations are strongly competitive against immigrants, while immigrants have little impact on residents. Finally, statistical models showed high population growth rates of resident cells in one experiment but not in the other, suggesting that Ap experiences relatively "good" and "bad" periods for population growth. This picture of Ap dynamics conforms to commonly held, but rarely demonstrated, expectations of microbe dynamics in nature. It also highlights the importance of local processes, as opposed to immigration, in determining the abundance and dynamics of microbes on surfaces in terrestrial systems.