Arbuscular mycorrhizal fungi (AMF) play vital roles in plant growth and rhizosphere microbiome assembly. Tree peony (Paeonia sect. Moutan DC.) is an economically valuable perennial crop, yet the symbiotic mechanisms between it and native AMF remain poorly understood. In this study, we surveyed the rhizosphere AMF community of wild P. ostii from its native habitat, and isolated two dominant species: Funneliformis mosseae and Claroideoglomus etunicatum. Inoculation with these AMF significantly improved root development and leaf photosynthetic efficiency. Furthermore, the promotion involved a novel pathway whereby carotenoid cleavage dioxygenase 4 (PoCCD4) mediated strigolactone and abscisic acid homeostasis in P. ostii roots. Beyond direct effects on host plant growth, AMF inoculation fine-tuned rhizosphere microbiota composition, reinforcing host-driven assembly and favoring beneficial consortia without altering overall diversity. Correlation analyses revealed that the AMF-shaped microenvironment established a disease-suppressive network linked to soil nutrient dynamics and phytohormone profiles. This study elucidates the interaction mechanisms between native AMF and P. ostii, uncovers their co-adaptive relationships, and offers a scientific basis for developing AMF inoculants for sustainable tree peony cultivation.