Translocation of elite cultivars across distinct climatic regions often induces transplantation shock. Although the rhizosphere microbiome can facilitate host acclimation, the underlying functional mechanisms remain unclear. Here, we investigated microbiome-mediated adaptation in “Hongdeng” sweet cherry (Prunus avium L.) moved from a humid coastal region (Dalian, DL) to a semi-arid inland habitat (Hohhot, HS). We integrated plant physiological assays, metagenomic sequencing, and structural equation modeling (SEM) to compare the source population (DL), the introduced population (HS), and a locally acclimated reference cultivar (“Summit”, HSY). The introduced trees adjusted physiologically to the semi-arid environment by elevating proline levels and antioxidant enzyme activities. Although environmental stress reduced microbial alpha diversity, the core taxonomic framework persisted. Community assembly analysis indicated that the semi-arid climate intensified environmental filtering. Network analysis identified Sphingomonas as a keystone taxon; notably, it maintained a highly connected topological role despite a stable relative abundance. Furthermore, structural equation modeling showed that the environmental stress index positively correlated with the upregulation of microbial DNA repair pathways (R = 0.81, p < 0.001). Ultimately, the SEM demonstrated that environmental stress primarily shapes microbial functional profiles rather than driving species turnover, thereby contributing to host adaptation. The successful establishment of introduced sweet cherry in semi-arid regions is tied more closely to rhizosphere functional plasticity than to taxonomic restructuring. These findings highlight the role of the keystone taxon Sphingomonas in maintaining rhizosphere homeostasis, offering a theoretical framework for targeted microbiome engineering to mitigate transplant shock and enhance crop resilience.