Wound-associated infections represent an arduous global healthcare challenge, especially in the "post-antibiotic" era, necessitating the development of advanced antimicrobial dressing materials that simultaneously dictate the use of rapid yet effective disinfection, low drug resistance and side effects, and the potency to foster tissue healing. Nanoantimicrobial-armored nanostructured functional dressing systems have piqued extensive interest to satisfy these criteria. Herein, fusing electrospinning nanotechnology and an emerging photo−chemo synergistic sterilization paradigm, a smart "all-in-one" multifunctional wound-managing dressing platform was constructed, through incorporating photochemically active nanocrystalline cuprous oxide (Cu 2 O) into modified polycaprolactone (mPCL) electrospun fibrous mats. The resulting materials were systematically characterized pertaining to physiochemical analysis, photoabsorption and photocurrent measurements, and photocatalytic reactive oxygen species (ROS) generation. The capability of this nanoplatform to elicit rapid, photoactivated, catalytically augmented bacterial disinfection was corroborated, displaying ∼99−100% broad-spectrum antibacterial efficacies against Staphylococcus aureus and Escherichia coli in 25 min. Benefiting from the release of Cu 2+ , mPCL-Cu 2 O impairs bacterial contamination even under dark conditions. Furthermore, these materials also exhibited favorable in vitro/-ovo biocompatibility toward NIH3T3 fibroblasts, red blood cells, and chick chorioallantoic membrane, alongside appreciable pro-healing capacity in bridging scratch-based wounds, which could be attributed to nanofiber-afforded biomimetic topography and controllable liberation of micronutrient Cu ions. This study provides insights into the design and fabrication of simple yet smart antibacterial nanoplatforms for biomedical applications.