Rhizosphere microbes affect plant performance, including plant resistance against insect herbivores; yet, a direct comparison of the relative influence of rhizosphere microbes vs. plant genotype on herbivory levels and on metabolites related to defense is lacking. In the crucifer Boechera stricta, we tested the effects of rhizosphere microbes and plant genotype on herbivore resistance, the primary metabolome, and select secondary metabolites. Plant populations differed significantly in the concentrations of 6 glucosinolates (GLS), secondary metabolites known to provide herbivore resistance in the Brassicaceae. The population with lower GLS levels experienced ~60% higher levels of aphid (Aphis spp.) attack; no association was observed between GLS and damage by a second herbivore, flea beetles (Altica spp.). Rhizosphere microbiome (disrupted vs. intact native microbiome) had no effect on plant GLS concentrations. However, aphid number and flea beetle damage were respectively ~3-fold and 7-fold higher among plants grown in the disrupted vs. intact native microbiome treatment. These differences may be attributable to shifts in primary metabolic pathways previously implicated in host defense against herbivores, including increases in pentose and glucoronate interconversion among plants grown with an intact microbiome. Further, native microbiomes with distinct community composition (as estimated from 16s rRNA amplicon sequencing) differed 2-fold in their effect on host plant susceptibility to aphids. The findings suggest that rhizosphere microbes, including distinct native microbiomes, can play a greater role than plant genotype in defense against insect herbivores, and act through metabolic mechanisms independent of plant genotype.