In a wake of shifting climatic scenarios, plants are frequently forced to undergo a spectrum of abiotic and biotic stresses at various stages of growth, many of which have a detrimental effect on production and survival. Naturally, microbial consortia partner up to boost plant growth and constitute a diversified ecosystem against abiotic stresses. Despite this, little is known pertaining to the interplay between endophytic microbes which release phytohormones and stimulate plant development in stressed environments. In a lab study, we demonstrated that an endophyte isolated from the Kargil region of India, a Fusarium equiseti strain K23-FE, colonizes the maize hybrid MAH 14 - 5, promoting its growth and conferring polyethylene glycol (PEG)-induced osmotic stress tolerance. To unravel the molecular mechanism, maize seedlings inoculated with endophyte were subjected to comparative transcriptomic analysis. In response to osmotic stress, genes associated with metabolic, photosynthesis, secondary metabolites, and terpene biosynthesis pathways were highly upregulated in endophyte enriched maize seedlings. Further, in a greenhouse experiment, maize plants inoculated with fungal endophyte showed higher relative leaf water content, chlorophyll content, and antioxidant enzyme activity such as polyphenol oxidase (PPO) and catalase (CAT) under 50% field capacity conditions. Osmoprotectant like proline were higher and malondialdehyde content was reduced in colonized plants. This study set as proof of concept to demonstrate that endophytes adapted to adverse environments can efficiently tweak non-host plant responses to abiotic stresses such as water deficit stress via physiological and molecular pathways, offering a huge opportunity for their deployment in sustainable agriculture.