Abstract Insect herbivory is pervasive in plant communities, but its impact on microbial plant colonizers is not well-studied in natural systems. By calibrating sequencing-based bacterial detection to absolute bacterial load, we find that the within-host abundance of most leaf microbiome (phyllosphere) taxa colonizing a native forb is amplified within leaves impacted by insect herbivory. Herbivore-associated bacterial amplification reflects community-wide compositional shifts towards lower ecological diversity, but the extent and direction of such compositional shifts can be interpreted only by quantifying absolute abundance. Experimentally eliciting anti-herbivore defenses reshaped within-host fitness ranks among Pseudomonas spp. field isolates and amplified a subset of putative P. syringae phytopathogens in a manner causally consistent with observed field-scale patterns. Herbivore damage was inversely correlated with plant reproductive success and was highly clustered across plants, which predicts tight co-clustering with putative phytopathogens across hosts. Insect herbivory may thus drive the epidemiology of plant-infecting bacteria as well as the structure of a native plant microbiome by generating variation in within-host bacterial fitness at multiple phylogenetic and spatial scales. This study emphasizes that “non-focal” biotic interactions between hosts and other organisms in their ecological settings can be crucial drivers of the population and community dynamics of host-associated microbiomes.