Fungi are promising materials for soil metal bioextraction and thus biomining. Here, a macrofungi-based system was designed for rapid cadmium (Cd) removal from alkaline soil. The system realized directed and rapid fruiting body development for subsequent biomass harvest. The Cd removal efficiency of the system was tested through a pot culture experiment. It was found that aging of the added Cd occurred rapidly in the alkaline soil upon application. During mushroom growth, the soil solution remained considerably alkaline, though a significant reduction in soil pH was observed in both Cd treatments. Cd and dissolved organic carbon (DOC) in soil solution generally increased over time and a significant correlation between them was detected in both Cd treatments, suggesting that the mushroom‒substratum system has an outstanding ability to mobilize Cd in an alkaline environment. Meanwhile, the growth of the mushrooms was not affected relative to the control. The estimated Cd removal efficiency of the system was up to 12.3% yearly thanks to the rapid growth of the mushroom and Cd enrichment in the removable substratum. Transcriptomic analysis showed that gene expression of the fruiting body presented considerable differences between the Cd treatments and control. Annotation of the differentially expressed genes (DEGs) indicated that cell wall sorption, intracellular binding, and vacuole storage may account for the cellular Cd accumulation. In conclusion, the macrofungi-based technology designed in this study has the potential to become a standalone biotechnology with practical value in soil heavy metal removal, and continuous optimization may make the system useful for biomining.