Microorganisms play a pivotal role in transforming and making phosphorus (P) available in soil through various mechanisms. However, their specific contributions to alleviating P limitation and enhancing P utilization efficiency in plants within the context of a P-deficient karst ecosystem remains unclear. In this study, eco-stoichiometric methods were employed to evaluate the P utilization efficiency of plants grown in the surveyed karst forest located in Guizhou Province, China. Metagenomic sequencing was utilized to further explore the functional genes and microorganisms involved in soil P cycling. The N:P ratio for 18 out of the 20 surveyed plants exceeded 16, indicating widespread P limitation in karst plants. Among them, plants with high P utilization efficiencies (Nandina domestica Thunb.; Mahonia bodinieri Gagnep.; Pyracantha fortuneana (Maxim.) Li) exhibited higher relative abundances of genes involved in soil P cycling compared to plants with low P utilization efficiencies (Tirpitzia sinensis (Hemsl.) Hallier f.; Albizia kalkora (Roxb.) Prain; Morella rubra Lour.), indicating greater potentials within their rhizosphere microbiomes for soil P transformation. The relative abundance of these functional genes had a significant and positive effect on plant P utilization efficiencies. Structural equation modeling further indicated that microbial P cycling gene abundance directly drove the increase in plant P utilization efficiencies. Specifically, genes involved in soil organic P mineralization (G6PD, suhB, phoD, ppx) and the P uptake and transform system (pstS, pstA, pstB, pstC) contributed to the enhancement of plant P utilization efficiencies. Soil microbial communities involved in P cycling were predominately attributed to Proteobacteria (45.16%–60.02%), Actinobacteria (9.45%–25.23%), and Acidobacteria (5.90%–9.85%), although their contributions varied among different plants. The rhizosphere functional microbial community can thus alleviate P limitation in karst plants, thereby enhancing plant P utilization efficiencies. This study investigated the strong synergism between karst plants and rhizosphere microorganisms and their associated underlying mechanisms from genetic and microbial perspectives.