The periosteum plays a crucial role in both bone development and the healing process of bone fractures. However, few studies have focused on developing artificial periosteum due to the complexity of its construction and the biological risks for clinical practice. To address this issue, we proposed a strategy for the fabrication of a photocrosslinkable natural hydrogel nanofibrous membrane (SFMA-Lap@AcBP) based on methacrylated silk fibroin (SFMA), photoinitiator (Lap), acrylate bisphosphonate (AcBP) through combining electrospinning technology with hydrogel, mimicking the structure and function of periosteum to promote bone regeneration. AcBP were covalently attached to the SFMA hydrogel nanofibrous membrane via conjugation. With the degradation of SFMA-Lap@AcBP hydrogel nanofibrous membrane, the released BP-grafted derivates could promote bone regeneration. Moreover, SFMA-Lap@AcBP hydrogel membranes were found to be able to trap metal ions such as Mg2+ and Ca2+in vivo, which might play a synergistic role in inducing complete bone regeneration. Furthermore, the hydrogel membranes had excellent cytocompatibility. They could imitate the microenvironment of the extracellular matrix, thereby offering structural and biochemical cues for the adhesion, proliferation, and differentiation of cells, without the need of exogenous cells or inductive growth factors, resulting in a facilitated osteogenesis. After implanting membranes into a cranial periosteal and bone defect in rats, both the amount and quality of new bone in the SFMA-Lap@AcBP group were found to be higher than those in the other groups. Therefore, the hydrogel membrane bionic periosteum was efficient and versatile in inducing bone regeneration, providing a potential strategy to address clinical issues.