Cancer cells, both within a developing tumor and upon entering the circulation to undergo metastatic spread, encounter a variety of stresses and thus require mechanisms to compensate for these challenges in order to survive. Here we describe a novel signaling complex that involves the small GTPase Cdc42 and Dock7, a Guanine Nucleotide Exchange Factor (GEF) and a unique Cdc42-effector, which plays a previously unappreciated role in the regulation of AKT and mTOR activity. The expression level of Dock7 is upregulated in triple-negative breast cancers and predicts an unfavorable prognosis in liver cancer patients. We show that Dock7 is essential for the transformed properties and survival of several cancer cell lines and that this appears to be linked to its ability to interact with Akt, mTOR, and other mTOR signaling and regulatory partners including the TSC1/TSC2 complex, as detected in co-immunoprecipitation assays and Proximity Ligation Assays (PLA). We further demonstrate that the serum starvation of HeLa cells results in the stress-dependent phosphorylation of Akt at Ser473 and an accompanying activation of a rapamycin-sensitive mTORC1-like activity that is dependent upon Cdc42 but does not require Raptor. Serum-starved Dock7 Knock-out cells failed to promote Akt phosphorylation at Ser473 nor activate its downstream signaling effectors, thus exhibiting greatly diminished survival potential and increased cell death, compared to wild-type cells. We demonstrate that Dock7 preferentially interacts with the active form of AKT and that this interaction is enhanced in serum-deprived conditions. Interestingly, we found that upon genetic ablation of Dock7, the colocalization between AKT and its main phosphatase, PHLPP, increases. Finally, we identified the DHR1 domain of Dock7, which has not previously been shown to have any catalytic activity, to be responsible for maintaining AKT in an activated state when cells are stressed by serum deprivation. Taken together, our findings suggest that Dock7 plays a previously unappreciated signaling role by protecting AKT from being de-phosphorylated and enabling a tonic activation of mTORC1-like activity that prevents cancer cells from undergoing apoptosis during stressful conditions. These results now identify Dock7 as a potential new therapeutic target in cancers where AKT activation is essential for tumor cell survival.