The Gram-negative opportunistic pathogen Pseudomonas aeruginosa is endowed with intrinsic resistance to antibiotics. It is essential to explore alternative techniques to supplement the arsenal of methods to kill drug-resistant bacteria. Herein, we established an "on-demand" nanoplatform based on acid-degradable scaffolds by conjugating glycomimetic-based galactose ligands to target a key lectin on P. aeruginosa and guanidine moieties. This nanoplatform could capture bacteria through ligand-receptor interactions and electrostatic interactions, and subsequently reactive oxygen species produced by entrapped photodynamic agent Ce6 under light irradiation eliminated drug-resistant P. aeruginosa and its biofilm. Approximately 95% of the planktonic bacteria were killed and more than 70% of the biofilm was disrupted under light irradiation. This strategy of copolymer modification could improve the biocompatibility and therapeutic efficiency levels of antibacterial therapeutics through the targeting of function. Hence, utilizing this smart nanoplatform may be of significance in developing new strategies to solve the growing problem of bacterial resistance.