In light of the limited resources of phosphorus (P) fertilizer, investigating the response of organic P (Po)-mineralizing microbial communities on the resource supply can be an avenue to optimize P recycling in agricultural systems. The alkaline phosphomonoesterase (alkaline PAse)-encoding gene PhoD is universally occurring in soil microorganisms. Here we collected 102 soil samples from Chinese agricultural fields to explore the effect of resource supply on the community of phoD-harboring bacteria. The relationships between the community diversity and soil organic carbon (SOC), total nitrogen (TN) and available Po concentration were fitted to the linear and quadric models suggested by the resource competition theory as well as the Michaelis-Menten model suggested by the metabolic theory of ecology. The results revealed that the response of phoD-harboring bacterial diversity to SOC and TN was likely related to the resource competition theory, with highest diversity at moderate SOC and TN concentration. In contrast, the phoD diversity increased with increasing available Po until the stationary value, which was consistent with the metabolic theory of ecology. Random forest models and multiple regression tree analyses identified the Po availability as the most important predictor on the variation of the phoD-harboring bacterial diversity and network topological features prior to the climate, soil texture, pH and all tested soil nutrient variables. This study highlights the critical role that Po plays in structuring phoD-harboring bacterial communities. Furthermore, for the first time, we correlated functional gene diversity to the corresponding enzymatic substrate availability from a metabolic theory perspective, confirming that the relationship follows the Michaelis-Menten model which was well known to predict the substrate regulation on the rate of enzymatic reactions.