The aim of the current study was to isolate endophytes from the roots of Rhazya stricta and assess their potential to improve the growth of drought-stressed sunflower seedlings. The potential role of the isolated endophytic fungus was initially screened by using two rice varieties (mutant rice cultivar Waito-C: Gibberellins deficient; and Dongji byeo: Gibberellins-producing normal cultivar). A significant (p < 0.05) increase in various growth attributes of both rice varieties associated with one of the isolates i.e., N4 was noticed. Furthermore, the N4 isolate was tested for its role in improving the agronomic attributes of sunflowers under drought stress. The symbiotic association significantly (p < 0.05) improved the host growth and protection from PEG-induced drought stress. The drought mitigation in N4-associated sunflower seedlings can be linked with the regulation of phytohormones, stress-related metabolites, low-molecular-weight proteins and sugars, and scavenging of reactive oxygen species (ROS). Microscopic analysis revealed that the potent endophytic fungal strain consisted of thin and hyaline hyphae, forming dense olive-green mycelia (4–5 cm in dm) with black flask-shaped fruiting bodies. Based on the ITS sequence homology and phylogeny, the strain was identified as Fusarium proliferatum (MG251448). The results of this study concluded that this phytohormone-secreting endophyte can improve crop productivity in dry areas where drought stress is the main challenge faced by crops.