Photoactivated pesticides (PPs) have photodynamic antimicrobial activities and show good environmental compatibility and slow resistance development. However, the disadvantages of easy aggregation, short duration, and low efficiency seriously restrict the efficient application of PPs. Hollow mesoporous copper sulfide nanoparticles (HMCuS NPs) with unique optical properties show photodynamic antimicrobial activity under light irradiation, which are considered smart drug delivery carriers due to their good water dispersivity and high drug encapsulation surface area. Herein, novel acid-responsive photoactivated pesticide nanocapsules (PPs@HMCuS-CTS NPs) were established by electrostatically coating HMCuS NPs loaded with PPs (curcumin and physcion) with chitosan (CTS). The results showed that the obtained nanocapsules had desirable water dispersivity (PDI0.25) and acid-responsive release properties. The antimicrobial activity of PPs@HMCuS-CTS NPs under light irradiation was more than 1.47 times those of PPs alone and the mixture of PPs and HMCuS NPs due to the synergistic photodynamic antimicrobial activity. Rainfastness, safety assessment, and genotoxicity evaluation demonstrated that the PPs@ HMCuS-CTS NPs deposited more than 1.28 times PPs on plant foliage without any damage to the crop. Therefore, acid-responsive photoactivated pesticide nanocapsules based on HMCuS NPs have the potential to be an efficient and safe pesticide delivery system.