Conservation of ecological communities requires deepening our understanding of genetic diversity patterns and drivers at community-wide scales. Here we use seascape genetic analysis of a diversity metric, allelic richness, for 47 reef species sampled across 13 Hawaiian Islands to empirically demonstrate that large reefs high in coral cover harbor the greatest genetic diversity on average. We found that a species’ life history (e.g., depth range and herbivory) mediates response of genetic diversity to seascape drivers in logical ways. Further, a metric of combined multi-species allelic richness showed strong coupling to species richness and habitat area, quality and stability that few species showed individually. We hypothesize that macroecological forces and species interactions, by mediating species turnover and occupancy and thus a site’s mean effective population size, influence the aggregate genetic diversity a site, potentially allowing it to behave as an apparent emergent trait that is shaped by the dominant seascape drivers. The results highlight inherent feedbacks between ecology and genetics, raise concern that genetic resilience of entire reef communities is compromised by factors that reduce coral cover or available habitat, including thermal stress, and provide a foundation for new strategies for monitoring and preserving biodiversity of entire reef ecosystems.