Background/Question/Methods Drought is among the most destructive abiotic stresses, which is projected to adversely affect 50% of the arable lands by 2050. There is now increasing recognition that plant-associated microbial communities can significantly stimulate plant growth and enhance plant resistance to abiotic stresses. Sustained by root exudates, a plethora of microorganisms inhabit rhizosphere forming a complex ecological community that influences plant growth and productivity. The rhizobiome plays a significant role in plant health, effectively serving as a second plant genome. Microbiome inhabiting the rhizosphere (rhizobiome) are increasingly recognized to confer stress tolerance to ruderal plants, yet their ability to alleviate stress in crops is widely debated. Despite the assumed high potential, the effectiveness of consortia of beneficial rhizobiomes from ruderal plants to effectively cross-infect crop plants and provide the stress resilience remains largely unknown. We hypothesized that cross-inoculation of the rhizobiome from a stressed environment, rather than from an optimal growing environment, would better equip the crop plants to tolerate the environmental stress. Results/Conclusions . We monitored the drought tolerance of maize (Zea mays) as influenced by the cross-inoculation of rhizobiota from a congeneric ruderal grass Andropogon virginicus (andropogon-inoculum), and from an organic farm maintained under mesic condition (organic-inoculum). Across drought treatments (40% field capacity), maize that received andropogon-inoculum produced two-fold greater biomass. This drought tolerance translated to similar tissue metabolomic composition as that of the well-watered control (80% field capacity) and reduced oxidative damage despite a lower activity of antioxidant enzymes. The drought mitigation was associated with an increase in specific root length and surface area, and up-regulation of proteins related to glutathione metabolism and endoplasmic reticulum-associated degradation process in maize roots. Fungal taxa belonging to Ascomycota, Mortierellomycota, Archaeorhizomycetes, Dothideomycetes, and Agaricomycetes in andropogon-inoculum were identified as potential indicators contributing to drought tolerance of maize. Our study demonstrates a better path to utilize plant-rhizobiome associations to enhance drought tolerance in crops and indicates that the observed resilience could partly be mediated by altering crop root morphology and proteomics.