Chinese Cordyceps (Ophiocordyceps sinensis) and Xinjiang Cordyceps (Paraisaria gracilis) are related entomopathogenic fungi that occupy different elevations and habitats. Whether their holobiont architectures have diverged accordingly is unknown. In this hypothesis-generating study based on samples from single locations (Altai Mountains for Xinjiang Cordyceps and Nagqu, Tibet for Chinese Cordyceps), we compared the two species using amplicon sequencing, untargeted metabolomics, and comparative genomics. Chinese Cordyceps from the sampled site comprises a specialized parasitic fungus and host-adapted bacteria for nutrient acquisition. Xinjiang Cordyceps from the Altai site contains diverse saprotrophic fungi and a rhizosphere-like bacterial consortium enriched in oxidative defense and biofilm genes, a finding that may explain why its sclerotia remain intact for 3–5 years in this population. Metabolomic profiles distinguish the two species at these sites. Xinjiang Cordyceps shows upregulation of tyrosine and porphyrin pathways, and its bacterial community shows functional enrichment in the same pathways, suggesting cross-kingdom coordination. P. gracilis has lost many gene families, and the retained species-specific genes are linked to cell adhesion and acyltransferase activity. Xinjiang Cordyceps is not a simple substitute for Chinese Cordyceps but appears to represent a different ecological strategy shaped by genome streamlining and host–microbe coadaptation. Our findings generate testable hypotheses for future large-scale, multi-population investigations.