Although microbial systems are well suited for studying concepts in ecological theory, little is known about how microbial communities respond to long-term periodic perturbations beyond diel oscillations. Taking advantage of an ongoing microcosm experiment, we studied how methanotrophic microbial communities adapted to disturbances in energy input over a 20-day cycle period. Sequencing of bacterial 16S rRNA genes together with quantification of microbial abundance and ecosystem function were used to explore the long-term dynamics (510 days) of methanotrophic communities under continuous versus cyclic chemical energy supply. We observed that microbial communities appeared inherently well adapted to disturbances in energy input and that changes in community structure in both treatments were more dependent on internal dynamics than on external forcing. The results also showed that the rare biosphere was critical to seeding the internal community dynamics, perhaps due to cross-feeding or other strategies. We conclude that in our experimental system, internal feedbacks were more important than external drivers in shaping the community dynamics over time, suggesting that ecosystems can maintain their function despite inherently unstable community dynamics. IMPORTANCE Within the broader ecological context, biological communities are often viewed as stable and as only experiencing succession or replacement when subject to external perturbations, such as changes in food availability or the introduction of exotic species. Our findings indicate that microbial communities can exhibit strong internal dynamics that may be more important in shaping community succession than external drivers. Dynamic "unstable" communities may be important for ecosystem functional stability, with rare organisms playing an important role in community restructuring. Understanding the mechanisms responsible for internal community dynamics will certainly be required for understanding and manipulating microbiomes in both host-associated and natural ecosystems.