Trichoderma, a highly abundant soil fungus, may benefit plants, yet it remains understudied in sorghum (Sorghum bicolor). In this study, sorghum plants were cultivated for five weeks in soil pots with or without the inoculation of T. afroharzianum T22. We found that plants inoculated with T. afroharzianum T22 exhibited significant increases in growth parameters and nutrient levels, demonstrating its beneficial role in sorghum. The split-root assay demonstrated that T. afroharzianum T22 is essential in both compartments of soil pots for promoting plant growth. This suggests that local signals from this fungus drive symbiotic benefits in sorghum. The RNA-seq analysis revealed the induction of genes responsible for mineral transport (such as nitrate and aquaporin transporters), auxin response, sugar assimilation (hexokinase), and disease resistance (thaumatin) in the roots of sorghum inoculated with T. afroharzianum T22. Microbial community analysis further unveiled the positive role of T. afroharzianum T22 in enriching Penicillium (ITS) and Streptomyces (16S) while reducing disease-causing Fusarium in the roots. The microbial consortium, consisting of enriched microbiomes from bacterial and fungal communities, showed disrupted morphological features in plants inoculated with T. afroharzianum T22 in the absence of S. griseus. However, this disruption was not observed in the absence of P. chrysogenum. These results suggest that S. griseus may act as a helper microbe in close association with T. afroharzianum T22 in the sorghum endosphere. This study provides the first comprehensive explanation of how T. afroharzianum T22 modulates host molecular determinants and endophytic helper microbes, thereby collectively promoting sorghum growth. These findings may encourage the formulation of a synthetic inoculum dominated by T. afroharzianum T22 to enhance growth and stress resilience in sorghum and other similar crops.