The rhizosphere is a hot spot of soil microbial activity and is largely fed by root exudation. The carbon (C) exudation flux, coupled with plant growth, is considered a strategy of plants to facilitate nutrient uptake. C exudation is accompanied by a release of nutrients. Nitrogen (N) and phosphorus (P) co-limit the productivity of the plant-microbial system. Therefore, the C:N:P stoichiometry of exudates should be linked to plant nutrient economies, plant functional traits (PFT) and soil nutrient availability. We aimed to identify the strongest links in C:N:P stoichiometry among all rhizosphere components. A total of eight grass species (from conservative to exploitative) were grown in pots under two different soil C:nutrient conditions for a month. As a result, a wide gradient of plant–microbial–soil interactions were created. A total of 43 variables of plants, exudates, microbial and soil C:N:P stoichiometry, and PFTs were evaluated. The variables were merged into four groups in a network analysis, allowing us to identify the strongest connections among the variables and the biological meaning of these groups. The plant–soil interactions were shaped by soil N availability. Faster-growing plants were associated with lower amounts of mineral N (and P) in the soil solution, inducing a stronger competition for N with microorganisms in the rhizosphere compared to slower-growing plants. The plants responded by enhancing their N use efficiency and root:shoot ratio, and they reduced N losses via exudation. Root growth was supported either by reallocated foliar reserves or by enhanced ammonium uptake, which connected the specific leaf area (SLA) to the mineral N availability in the soil. Rapid plant growth enhanced the exudation flux. The exudates were rich in C and P relative to N compounds and served to release surplus metabolic products. The exudate C:N:P stoichiometry and soil N availability combined to shape the microbial stoichiometry, and N and P mining. In conclusion, the exudate flux and its C:N:P stoichiometry reflected the plant growth rate and nutrient constraints with a high degree of reliability. Furthermore, it mediated the plant–microbial interactions in the rhizosphere.