In the context of severe burn injuries, the presence of excessive reactive oxygen species (ROS), prolonged microbial infection, and compromised angiogenesis can contribute to the metabolic reprogramming of macrophages, resulting in a dysregulated inflammatory response that hinders the healing process. In this study, cerium oxide nanoparticles (CeNPs) are encapsulated within a silk fibroin‐poly(e‐caprolactone) polymer to create an electrospun PSF/CeNPs nanofiber membrane (PSF/membrane). This membrane is further modified through the addition of an angiopoietin‐1 mimetic peptide, QHREDGS, resulting in the formation of QPSF/CeNPs (QHREDGS modified PSF/CeNPs membrane). In vitro assessments revealed that the QPSF/CeNPs displayed the intended ability to regulate ROS levels, favorable biocompatibility with cells, promoted endothelial cell attachment and growth, exhibited anti‐inflammatory properties through the modulation of macrophage phenotypes from M1 to M2, as well as pro‐angiogenetic and antibacterial effects. In vivo, the membrane dressing demonstrated an acceleration of burn wound healing, promotion of angiogenesis, downregulation of inflammatory factors, and enhancement of collagen deposition. This bioactive membrane dressing shows potential as a clinical therapy for promoting the regeneration of both acute and chronically damaged skin tissue.