Closely interacting microbial species pairs (e.g., predator and prey) can become coadapted via reciprocal natural selection. A fundamental challenge in evolutionary ecology is to untangle how coevolution in small species groups affects and is affected by biotic interactions in diverse communities. We conducted an experiment with a synthetic 30-species bacterial community where we experimentally manipulated the coevolutionary history of a ciliate predator and one bacterial prey species from the community. Altering the coevolutionary history of the focal prey species had little effect on community structure or carrying capacity in the presence or absence of the coevolved predator. However, community metabolic potential (represented by per-cell ATP concentration) was significantly higher in the presence of both the coevolved focal predator and prey. This ecosystem-level response was mirrored by community-wide transcriptional shifts that resulted in the differential regulation of nutrient acquisition and surface colonization pathways across multiple bacterial species. Our findings show that the disruption of localized coevolution between species pairs can reverberate through community-wide transcriptional networks even while community composition remains largely unchanged. We propose that these altered expression patterns may signal forthcoming evolutionary and ecological change.