With its premium wood quality and resistance to pests, teak is a valuable tree species remarkably required for timber trading and agroforestry. The nursery stage of teak plantation needs critical care to warrant its long-term productivity. This study aimed to search for beneficial teak rhizosphere microbes and assess their teak-growth-promoting potentials during nursery stock preparation. Three teak rhizosphere/root-associated microbes, including two teak rhizobacteria (a nitrogen-fixing teak root endophyte-Agrobacterium sp. CGC-5 and a teak rhizosphere actinobacterium-Kitasatospora sp. TCM1-050) and an arbuscular mycorrhizal fungus (Claroideoglomus sp. PBT03), were isolated and used in this study. Both teak rhizobacteria could produce in vitro phytohormones (auxins) and catalase. With the pot-scale assessments, applying these rhizosphere microbes in the form of consortia offered better teak-growth-promoting activities than the individual applications, supported by significantly increased teak seedling biomass. Moreover, teak-growth-promoting roles of the arbuscular mycorrhizal fungus were highly dependent upon the support by other teak rhizobacteria. Based on our findings, establishing the synergistic interactions between beneficial rhizosphere microbes and teak roots was a promising sustainable strategy to enhance teak growth and development at the nursery stage and reduce chemical inputs in agroforestry.