Plant–soil feedback (PSF) may influence plant–insect interactions. Although plant defense differs between shoot and root tissues, few studies have examined root-feeding insect herbivores in a PSF context. We examined here how plant growth and resistance against root-feeding Delia radicum larvae was influenced by PSF. We conditioned soil with cabbage plants that were infested with herbivores that affect D. radicum through plant-mediated effects: leaf-feeding Plutella xylostella caterpillars and Brevicoryne brassicae aphids, root-feeding D. radicum larvae, and/or added rhizobacterium Pseudomonas simiae WCS417r. We analyzed the rhizosphere microbial community, and in a second set of conspecific plants exposed to conditioned soil, we assessed growth, expression of defense-related genes, and D. radicum performance. The rhizosphere microbiome differed mainly between shoot and root herbivory treatments. Addition of Pseudomonas simiae did not influence rhizosphere microbiome composition. Plant shoot biomass, gene expression, and plant resistance against D. radicum larvae was affected by PSF in a treatment-specific manner. Soil conditioning overall reduced plant shoot biomass, Pseudomonas simiae-amended soil causing the largest growth reduction. In conclusion, shoot and root insect herbivores alter the rhizosphere microbiome differently, with consequences for growth and resistance of plants subsequently exposed to conditioned soil.