Abstract Plant economics, the way plants allocate and utilize resources, affect multiple soil processes through interactions with root and associated microbial communities. However, the interplay between plant economics and microbial ecological strategies remains poorly understood, which is crucial for integrated manipulation of plant‐ and microbe‐mediated functions in mitigating climate change and sustaining soil health. We used a field experiment with 11 cover crop species grown monocultures in the same base soil to test whether microbial ecological strategies are associated with plant economic strategies and if their interactions are linked to soil functions. A principal component analysis (PCA) was performed on root and leaf traits to identify the loadings of cover crop species on the plant trait space. Metagenomic analysis of rhizosphere microbial communities was conducted to infer their ecological strategies based on genetically encoded community‐aggregated traits. We found a synchronous relationship between the conservation gradient of plant economic strategies and the trade‐offs in microbial ecological strategies. Conservative plant strategists, such as Lolium multiflorum, Triticum turgidum and Brassica juncea, fostered microbial communities characterized by high growth yield potentials (Y‐strategies). This included increased microbial carbon fixation pathways, citrate cycle, ribosome and valine, leucine and isoleucine biosynthesis. As a result, microbial metabolic efficiency improved, shown by higher microbial biomass carbon content and a lower metabolic quotient (qCO2), led to enhanced soil organic carbon accumulation. In comparison, acquisitive plants like Astragalus sinicus, Vicia villosa, Trifolium incarnatum and Medicago sativa stimulated microbial resource‐acquisition strategies (A‐strategies). This included enhanced bacterial chemotaxis, secretion systems, biotin metabolism and cell motility pathways, which in turn increased soil exoenzyme activity and accelerated soil nitrogen mineralization. Consequently, these species enhanced soil nitrogen availability and had substantial feedbacks on subsequent main crop productivity. Synthesis. This study demonstrates how plant economic strategies influence the balance between different microbial ecological strategies, specifically the trade‐offs in Y‐ and A‐strategies. These interactions exert control over carbon and nitrogen dynamics in the soil ecosystem. The findings provide insights for implementing nature‐based solutions to improve agroecosystem management practices.