Marginal soils arise due to various industrial and agricultural practices reducing crop productivity. Pseudomonas sp. TLC 6-6.5-4 is a free-living multiple-metal-resistant plant-growth-promoting bacteria (PGPB) isolated from Torch Lake sediment that promotes maize growth and nutrient uptake. In this study, we examined both PGPB-soil and PGPB-plant interactions. PGPB inoculation resulted in significant increase in maize biomass. Soil inoculation before sowing seeds and coating seeds with the PGPB resulted in higher copper uptake by maize compared to other methods. The PGPB-soil interaction improved phosphorus uptake by maize and led to significant decrease in organic bound copper in marginal soil and a notable increase in exchangeable copper. PGPB improved soil health based on soil enzyme activities. Metabolomic analysis of maize revealed that PGPB inoculation upregulated photosynthesis, hormone biosynthesis, and tricarboxylic acid cycle metabolites. Proteomic analysis identified upregulation of proteins related to plant development and stress response. Further, the activity of antioxidant enzymes and total phenolics decreased in plants grown in marginal soil suggesting alleviation of metal stress in presence of PGPB. The ability of PGPB to modulate interconnected biochemical pathways could be exploited to increase crop productivity in marginal soils, phytoremediation of metal contaminated soils, and organic agriculture.