Plant growth-promoting rhizobacteria (PGPR) provide critical ecological value in sustainable agriculture by enhancing plant growth and stress tolerance through improved nutrient acquisition and increased environmental adaptability. As a versatile genus of PGPR, Streptomyces shows great potential for promoting plant growth. However, the molecular mechanisms by which Streptomyces regulates plant root development remain largely unclear. In this study, we explored the molecular basis associated with wheat root developmental responses to Streptomyces pactum Act12 using pot experiments combined with multi-omics approaches. The pot experiment demonstrated that Act12 treatment significantly increased wheat biomass and enhanced total root length (44.6%), root surface area (73.3%), root diameter (34.0%), and root tip number (66.6%). Integrated transcriptomic and metabolomic analyses suggested that Act12 treatment was associated with altered auxin signaling and coordinated changes in carbohydrate metabolism, the TCA cycle, and sterol biosynthesis. These multi-omics signatures provide hypotheses for how Act12 may contribute to root developmental regulation in wheat.