The Mediterranean fruit fly (medfly) (Ceratitis capitata) lays eggs in fruits, where larvae subsequently develop, causing largescale agricultural damage. Within its digestive tract, the fly supports an extended bacterial community thatis composed of multiple strains of a variety of enterobacterial species. Most of these bacteria appear to be functionally redundant, with most strains sustaining diazotrophy and/or pectinolysis. At least some of these bacteria were shown tobe vertically inherited, but colonization, structural, and metabolic aspects of the community's dynamics have not beeninvestigated. We used fluorescent in situ hybridization, metabolic profiling, plate cultures, and pyrosequencing to showthat an initial, egg-borne, diverse community expands throughout the fly's life cycle. While keeping "core" diazotrophic and pectinolytic functions, it also harbors diverse and fluctuating populations that express varied metabolic capabilities. We suggest that the metabolic and compositional plasticity of the fly's microbiota provides potential adaptive advantages to the medfly host and that its acquisition and dynamics are affected by mixed processes that include stochastic effects, host behavior, and molecular barriers.