Terrestrial plants serve as large and diverse habitats for a wide range of pathogenic and nonpathogenic microbes, yet these communities are not well described and little is known about the effects of plant defense on microbial communities in nature. We designed a field experiment to determine how variation in two plant defense signaling pathways affects the size, diversity, and composition of the natural endophytic and epiphytic bacterial communities of Arabidopsis thaliana. To do this, we provide an initial characterization of these bacterial communities in one population in southwestern Michigan, United States, and we compare these two communities among A. thaliana mutants deficient in salicylic acid (SA) and jasmonic acid (JA) signaling defense pathways, controls, and plants with artificially elevated levels of defense. We identified 30 distinct bacterial groups on A. thaliana that differ in colony morphology and 16S rRNA sequence. We show that induction of SA-mediated defenses reduced endophytic bacterial community diversity, whereas plants deficient in JA-mediated defenses experienced greater epiphytic bacterial diversity. Furthermore, there was a positive relationship between total community size and diversity, indicating that relatively susceptible plants should, in general, harbor higher bacterial diversity. This experiment provides novel information about the ecology of bacteria on A. thaliana and demonstrates that variation in two specific plant-signaling defense pathways can influence bacterial diversity on plants.