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The development of new approaches for the treatment of the increasingly antibiotic-resistant pathogen <i>Pseudomonas aeruginosa</i> was targeted by enhancing the effect of local antimicrobial photodynamic therapy (aPDT) using poly(ethylene glycol)-<i>block</i>-poly(lactic acid) (PEG₁₁₄-<i>block</i>-PLA_x) nanocarriers that were loaded with a ruthenium-based photosensitizer (PS). The action of tris(1,10-phenanthroline) ruthenium (II) bis(hexafluorophosphate) (RuPhen3) encapsulated in PEG₁₁₄-<i>block</i>-PLA_x micelles and vesicles was shown to result in an appreciable aPDT inactivation efficiency against planktonic <i>Pseudomonas aeruginosa</i>. In particular, the encapsulation of the PS, its release, and the efficiency of singlet oxygen (¹O₂) generation upon irradiation with blue light were studied spectroscopically. The antimicrobial effect was analyzed with two strains of <i>Pseudomonas aeruginosa</i>. Compared with PS-loaded micelles, formulations of the PS-loaded vesicles showed 10 times enhanced activity with a strong photodynamic inactivation effect of at least a 4.7 log reduction against both a <i>Pseudomonas aeruginosa</i> lab strain and a clinical isolate collected from the lung of a cystic fibrosis (CF) patient. This work lays the foundation for the targeted eradication of <i>Pseudomonas aeruginosa</i> using aPDT in various medical application areas.