Climate change has reshaped global weather patterns and intensified extreme events, with drought and soil salinity negatively impacting the yield and quality of crop production. To mitigate the detrimental effects of drought stress, the introduction of beneficial plant growth-promoting rhizobacteria (PGPR) has proven to be a promising approach. In this study, we evaluated a synthetic microbial community (SynCom) comprising bacterial strains belonging to the species Bacillus velezensis, Pseudomonas simiae, P. salmasensis, Glutamicibacter halophytocola, and Leclercia sp., which have been demonstrated to promote tomato growth both individually and collectively. The SynCom and most of its individual bacterial strains were shown to mitigate the detrimental effects of polyethylene glycol (PEG)-induced drought stress in vitro in Arabidopsis thaliana seedlings, either by reducing alterations in xylem elements or promoting the formation of new xylem strands. In a greenhouse trial, soil drenching with the SynCom and two individual strains, B. velezensis PSE31B and P. salmasensis POE54, improved the water stress response in soilless-grown tomato plants under a 40% reduced irrigation regime. Additionally, bacterial treatments positively influenced the diversity of rhizosphere bacterial communities, with distinct changes in bacterial composition, which suggest a treatment-specific interplay between the introduced strains and the native microbiome. These findings highlight the potential of microbial consortia and individual PGPR strains as sustainable tools to improve plant resilience to abiotic stresses.