Targeted bactericide nanosystems hold significant promise to improve the efficacy of existing antimicrobials for treatment of severe bacterial infections, minimizing the side effects and lowering the risk of antibiotic resistance occurrence. In this work, we developed antibody functionalized nanocapsules (NCs) containing antibacterial essential oil (EO) for selective and effective eradication of Staphylococcus aureus. Antibacterial EO NCs were produced via self-assembling nanoencapsulation in the plant-derived protein zein. The obtained EO NCs were decorated with aminocellulose to provide more reactive surface groups for carboxyl-to-amine immobilization of a specific against S. aureus antibody. The antibody-enabled EO NCs (Ab@EO NCs) demonstrated 2-fold higher bactericidal efficacy against the targeted bacterium compared to the pristine EO NCs at the same concentrations. The improved antibacterial effect of the Ab@EO NCs towards S. aureus was also confirmed in a real time assay by monitoring bacterial cells elimination using a quartz crystal microbalance. Furthermore, the Ab@EO selectively decreased the load and changed the cell morphology of the targeted S. aureus in a mixed inoculum with non-targeted P. aeruginosa. Applying the nanoformulated actives to an in vitro co-culture model of the bacteria and skin fibroblasts resulted in suppression of S. aureus growth, while preserving the human cells viability. The novel antibody-enabled antibacterial NCs showed potential to improve the treatment efficacy of staphylococcal infections, minimally affecting the beneficial microbiome and human cells.