The soilborne pathogen Ralstonia solanacearum is the causal agent of bacterial wilt and causes significant crop loss in the Solanaceae family. The pathogen first infects roots, which are a critical source of resistance in tomato (Solanum lycopersicum L.). Roots of both resistant and susceptible plants are colonized by the pathogen, yet rootstocks can provide significant levels of resistance. Currently, mechanisms of this 'root-mediated resistance' remain largely unknown. To identify the molecular basis of this resistance, we analyzed the genome-wide transcriptional response of roots of resistant 'Hawaii 7996' and susceptible 'West Virginia 700' (WV) tomatoes at multiple timepoints after inoculation with R. solanacearum. We found that defense pathways in roots of the resistant Hawaii 7996 are activated earlier and more strongly than roots of susceptible WV. Further, auxin signaling and transport pathways are suppressed in roots of the resistant variety. Functional analysis of an auxin transport mutant in tomato revealed a role for auxin pathways in bacterial wilt. Together, our results suggest that roots mediate resistance to R. solanacearum through genome-wide transcriptomic changes that result in strong activation of defense genes and alteration of auxin pathways.