Chronic wounds and their associated bacterial infections are major issues in modern health care systems. Therefore, antimicrobial resistance (AMR), treatment costs, and number of disability-adjusted life-years have gained more interest. Recently, photodynamic therapy emerged as an effective approach against resistant and naive bacterial strains with a low probability of creating AMR. In this study, needleless electrospinning was used to produce an indocyanine green (ICG) loaded poly(D,L-lactide) nanofibrous mesh as a photoresponsive wound dressing. The non-woven mesh had a homogeneous nanofibrous structure and showed long-term hydrolytic stability at different pH values. The antimicrobial activity was tested against several bacterial strains, namely Staphylococcus saprophyticus subsp. bovis, Escherichia coil DH5 alpha, and Staphylococcus aureus subsp. aureus. Upon irradiation with a laser of a specific wavelength (lambda = 810 nm), the bacterial viability was significantly reduced by 99.978% (3.66 log(10)), 99.699% (2.52 log(10)), and 99.977% (3.64 log(10)), respectively. The nanofibrous mesh showed good biocompatibility, which was confirmed by the proliferation of mouse fibroblasts (L929) on the surface and into deeper parts of the mesh. Furthermore, a favorable proangiogenic effect was observed in ovo using the chorioallantoic membrane assay. In general, it can be concluded that ICG loaded nanofibers as an innovative wound dressing represent a promising strategy against chronic wounds associated with skin infections.