High-Andean páramo ecosystems are characterized by harsh environmental conditions that shape the structure and functioning of plant-associated microbial communities. However, the ecological drivers underlying microbial functional organization across plant compartments remain poorly understood. In this study, we characterized the functional metagenomic profiles of rhizospheric soil, non-rhizospheric soil, and endophytic microbiomes associated with Azorella spp. in the Ecuadorian Llanganates National Park using shotgun metagenomic sequencing and metabolic pathway reconstruction with HUMAnN3 and MetaCyc. Functional diversity differed significantly among microbial compartments for all alpha diversity indices (FDR-adjusted p < 0.001), and beta diversity analyses showed that ecological compartment was the primary determinant of functional composition (PERMANOVA, R2 = 0.590, p = 0.001), whereas geographic location had no significant effect (R2 = 0.082, p = 0.393). Across all compartments, microbial communities shared a conserved metabolic core dominated by pathways involved in nucleoside and nucleotide biosynthesis, amino acid biosynthesis, cofactor and vitamin biosynthesis, and fatty acid and lipid biosynthesis, indicating high functional redundancy despite taxonomic differentiation. Differential abundance analyses identified 42 metabolic pathways that varied significantly among ecological compartments (FDR < 0.05), revealing compartment-specific metabolic specialization. Hierarchical clustering further demonstrated that endophytic communities were functionally distinct from soil-associated microbiomes, whereas rhizospheric and non-rhizospheric soils displayed greater functional similarity. Environmental analyses identified 345 significant associations between metabolic pathways and environmental variables after false discovery rate correction. Soil physicochemical properties, particularly potassium, iron, magnesium, calcium, manganese, and other exchangeable cations, were the strongest predictors of functional variation, whereas climatic and radiometric variables exerted comparatively weaker effects. Distance-based redundancy analysis confirmed that soil properties significantly explained microbial functional composition (Pseudo-F = 6.99, p = 0.001), with the first two constrained axes accounting for 89.9% of the explained variation. These findings demonstrate that microbial functionality in tropical high-Andean páramos is primarily structured by ecological compartment and soil physicochemical conditions rather than geographic location. The conservation of a shared metabolic backbone combined with compartment-specific functional specialization highlights the existence of a resilient microbial metabolic network that supports nutrient cycling, plant–microbe interactions, and ecosystem functioning under extreme mountain environments.