Using a phyllosphere model system, we demonstrated that the term carrying capacity, as it is commonly used in microbial ecology, needs to be understood as the sum of many local carrying capacities in order to better explain and predict the course and outcome of bacterial colonization of an environment. Using a green fluorescent protein-based bioreporter system for the quantification of reproductive success (RS) in individual Erwinia herbicola cells, we were able to reconstruct the contribution of individual immigrants to bacterial population sizes on leaves. Our analysis revealed that plant foliage represents to bacteria an environment where individual fate is determined by the local carrying capacity of the site where an immigrant cell lands. With increasing inoculation densities, the RS of most immigrants declined, suggesting that local carrying capacity under the tested conditions was linked to local nutrient availability. Fitting the observed experimental data to an adapted model of phyllosphere colonization indicated that there might exist three types of sites on leaves, which differ in their frequency of occurrence and local carrying capacity. Specifically, our data were consistent with a leaf environment that is characterized by few sites where individual immigrants can produce high numbers of offspring, whereas the remainder of the leaf offered an equal number of sites with low and medium RS. Our findings contribute to a bottom-up understanding of bacterial colonization of leaf surfaces, which includes a quantifiable role of chance in the experience at the individual level and in the outcome at the population level. © 2012 International Society for Microbial Ecology All rights reserved.