Soil microorganisms can influence the development of complex plant phenotypes, including resistance to herbivores. This microbiome-mediated plasticity may be particularly important for plant species that persist in environments with drastically changing herbivore pressure, for example over community succession. We established a 15-yr gradient of old-field succession to examine the herbivore resistance and rhizosphere microbial communities of Solidago altissima plants in a large-scale field experiment. To assess the functional effects of these successional microbial shifts, we inoculated S. altissima plants with microbiomes from the 2nd, 6th and 15th successional years in a glasshouse and compared their herbivore resistance. The resistance of S. altissima plants to herbivores changed over succession, with concomitant shifts in the rhizosphere microbiome. Late succession microbiomes conferred the strongest herbivore resistance to S. altissima plants in a glasshouse experiment, paralleling the low levels of herbivory observed in the oldest communities in the field. While many factors change over succession and may contribute to the shifts in rhizosphere communities and herbivore resistance we observed, our results indicated that soil microbial shifts alone can alter plants’ interactions with herbivores. Our findings suggest that changes in soil microbial communities over succession can play an important role in enhancing plant resistance to herbivores.