While the functions of vacuolar processing enzymes (VPE) in plant responses to pathogens are now better established, their possible roles against insect herbivores need validation. Inspired by an observation that betaVPE and deltaVPE represent the most highly upregulated transcripts in leaves of Solanum bulbocastanum and its backcross progenies that were highly resistant to the phloem-feeding green peach aphids (Myzus persicae), we used a reverse genetic approach in Arabidopsis to investigate whether T-DNA insertion mutants for specific betavVPE and deltaVPE loci would exhibit compromised defenses at the whole-plant, physiological, and molecular levels. We hypothesized that impaired expression of VPE genes would lead to hyper-susceptibility if VPE-mediated processes were essential for basal defenses, given that Arabidopsis is naturally susceptible. Compared to the wild-type, betaVPE and deltaVPE mutants exhibited an early onset of leaf curling and necrosis, rapid aphid population build-up, and significant physiological tissue injuries as a result of herbivory. This indicates that basal defenses were compromised by the loss-of-functions of either VPE-encoding gene. VPE co-expression networks were comprised of genes involved in sucrose metabolism and transport (AtSUC5, AtSUS3, and invertases), efflux and oxidative detoxification proteins, and modulators of gene-for-gene-type disease response linked to sucrose metabolism (AtSWEET13 and AtSWEET15). These results suggest that VPEs play a role in basal defenses by mediating mechanisms of detoxification and metabolite availability in host tissues to counteract the rapid depletion caused by the phloem sucker. These processes might be important as first line of defense to delay the progression of perturbations caused by herbivory.