CpG‐ODN induces cell survival, but the mechanism of its action remains elusive. Here we show that CpG‐ODN activates the TORC1 pathway in a DNA‐PKcs‐ and Akt‐ dependent manner. Loss of DNA‐PKcs impairs phosphorylation of Akt473S, mTOR2448S, and TORC1 effectors 4E‐BP1(65S), S6K(389T) and S6(235/236S) in response to CpG‐ODN, whereas lack of TLR9, MyD88 or IRAK4 only has a negligible effect in this phosphorylation process. Ablation of both Akt1 and Akt2 or inhibition of Akt abrogates TORC1 activation. As a consequence, deletion of DNA‐PKcs and inhibition of Akt and TORC1 results in failure of CpG‐ODN to dissociate 4E‐BP1 from eIF4E. Immunoprecipitation experimental results also show that DNA‐PKcs pre‐associates with mTOR, and CpG‐ODN stimulation enhances this association. Finally, DNA‐PKcs deficiency and TORC1 inhibition lead to a defect in CpG‐ODN‐ induced protection of cells against the anti‐leukemia agent vincristine. Overall, our findings indicate that the TORC1 pathway is downstream of the CpG‐ODN/DNA‐PKcs/Akt axis and its activation contributes to the CpG‐ODN‐ induced anti‐apoptotic function.