Phytophagous insects must contend with numerous secondary defense compounds that can adversely affect their growth and development. The gypsy moth (Lymantria dispar) is a polyphagous herbivore that encounters an extensive range of hosts and chemicals. We used this folivore and a primary component of aspen chemical defenses, namely, phenolic glycosides, to investigate if bacteria detoxify phytochemicals and benefit larvae. We conducted insect bioassays using bacteria enriched from environmental samples, analyses of the microbial community in the midguts of bioassay larvae, and in vitro phenolic glycoside metabolism assays. Inoculation with bacteria enhanced larval growth in the presence, but not absence, of phenolic glycosides in the artificial diet. This effect of bacteria on growth was observed only in larvae administered bacteria from aspen foliage. The resulting midgut community composition varied among the bacterial treatments. When phenolic glycosides were included in diet, the composition of midguts in larvae fed aspen bacteria was significantly altered. Phenolic glycosides increased population responses by bacteria that we found able to metabolize these compounds in liquid growth cultures. Several aspects of these results suggest that vectoring or pairwise symbiosis models are inadequate for understanding microbial mediation of plant-herbivore interactions in some systems. First, bacteria that most benefitted larvae were initially foliar residents, suggesting that toxin-degrading abilities of phyllosphere inhabitants indirectly benefit herbivores upon ingestion. Second, assays with single bacteria did not confer the benefits to larvae obtained with consortia, suggesting multi- and inter-microbial interactions are also involved. Our results show that bacteria mediate insect interactions with plant defenses but that these interactions are community specific and highly complex.