Tropical reef ecosystems lie at the interface of productive, populated terrestrial coastlines and unproductive, oligotrophic oceanic waters. Corals and other dominant reef organisms maintain complex symbiotic interactions with both surficial and planktonic aquatic microbial communities, but the processes defining the composition and life history of these communities are poorly understood. Because of the tight coupling between microbes and reef organisms, characterizing the ecology of bacteria and archaea in the waters bathing coral reefs is important in understanding reef ecosystem and community dynamics and predicting their response to environmental change. Here we present a suite of results illustrating how microbial abundance, community structure, and metabolism vary across tropical reef ecotones at multiple spatial and temporal scales. We show temporally-consistent spatial patterning of bacterioplankton abundance and community structure maintained across well-characterized hydraulic flowpaths, suggesting rapid and strong environmental selection for specialized microbial communities among reef habitats. Dissolved organic matter (DOM), the primary nutrient source for heterotrophic bacterioplankton, displays clear gradients among interacting oceanic and reef habitats, both in bulk concentration and fluorescence characteristics. Our culturing experiments illustrate how local differences in the source of natural DOM regulate the community structure and metabolic efficiency of bacterioplankton communities, implicating DOM dynamics as one factor structuring reef microbial communities. Finally, we present analysis of community structure variation within and among corals at the interface between planktonic and attached prokaryotic communities, demonstrating the maintenance of a striking difference in community structure of both bacteria and archaea between corals and the surrounding water.