Plant-growth promoting microbes (PGPM) are a viable alternative to traditional fertilizers for enhancing plant productivity and improving soil quality without environmental pollution. The use of PGPM in agriculture has been hampered by a lack of reproducible results and the difficulty of transferring this technology to the field. This inconsistent success primarily reflects competition or resistance of the original soil microbiome to inoculants, as well as the negative effects of management practices such as fertilization on plant interactions with the soil microbiome and the efficiency of ecosystem services delivered by PGPM. We were the first to circumvent this problem under field conditions by manipulating the soil microbiome to successfully obtain consistent, positive effects of inoculated microbes on plant productivity (Cipriano et al., 2016;https://doi.org/10.1093/femsec/fiw197). However, the influence of the indigenous soil microbiome on plants remains largely unknown. We propose to investigate this tripartite, PGPM-plant-soil microbiome interaction in plant quality and productivity using state-of-the-art ‘omics’ and bioinformatics approaches to investigate facilitation (positive interactions) and competition (negative interactions) by both microbes and PGPM within the plant realized niche following gradients of both soil diversity and nutrient availability. This research will facilitate the development of innovative methods for agricultural and horticultural starting material production using PGPM for sustainable crop production by combining techniques to reduce nutrient input and enhance the efficiency and long-lasting effects of PGPM. This research proposal will integrate approaches to obtain a fundamental understanding of these tripartite interactions in a smart microbiome engineered plant production system for sustainable high-quality crop production.