Similar to plant growth, soil carbon (C) cycling is constrained by the availability of nitrogen (N) and phosphorus (P). We hypothesized that stoichiometric control over soil microbial C cycling may be shaped by functional guilds with distinct nutrient substrate preferences. Across a series of rice fields spanning 5-25% soil C (N:P from 1:12 to 1:70), C turnover was best correlated with P availability and increased with experimental N addition only in lower C (mineral) soils with N:P⩽16. Microbial community membership also varied with soil stoichiometry but not with N addition. Shotgun metagenome data revealed changes in community functions with increasing C turnover, including a shift from aromatic C to carbohydrate utilization accompanied by lower N uptake and P scavenging. Similar patterns of C, N and P acquisition, along with higher ribosomal RNA operon copy numbers, distinguished that microbial taxa positively correlated with C turnover. Considering such tradeoffs in genomic resource allocation patterns among taxa strengthened correlations between microbial community composition and C cycling, suggesting simplified guilds amenable to ecosystem modeling. Our results suggest that patterns of soil C turnover may reflect community-dependent metabolic shifts driven by resource allocation strategies, analogous to growth rate-stoichiometry coupling in animal and plant communities.