AbstractThe lack of periosteum in bone allografts is considered a major cause of bone graft failure; however, the currently used artificial periosteum has failed to proactively adapt to its chronological role in the repair process. This study designed an adaptive periosteal system with dual‐response mechanisms to enable interactive angiogenic/osteogenic stimulation customized for inflammatory and anabolic stages of bone healing. Utilizing the enzymatic reactions and photodynamic properties of gold nanorod‐porous silicon, angiogenic peptides (QK) are released in response to matrix metalloproteinase 2 (MMP‐2), whereas bone‐forming peptides (BFP) are triggered by timed near‐infrared (NIR) irradiation, providing a portfolio of growth factors that match the dynamics of bone healing. The incorporation of such nanocarriers into a poly(N‐isopropyl acrylamide)/methacrylic acid gel (PNIPAM/GelMA) successfully formed a bionic periosteum that actively adapted to the function of the periosteum in different scenarios, resulting in more than doubled its ability to promote angiogenesis, stem cell migration, and osteogenesis compared to the controls. Furthermore, over 80% of the defects are covered with a new scab after the timed near‐infrared irradiation of large bone defects implanted with the system. The bionic periosteum actively mimicked the role of the periosteum in bone healing and offered a novel selection strategy for adaptability.