Many viruses affect or exploit the phosphatidylinositol-3-kinase (PI3K)–Akt– mammalian target of Rapamycin (mTOR) pathway, a crucial pro-survival signalling cascade. We report that this pathway was strongly activated in cells upon infection with the Old World alphavirus Semliki Forest virus (SFV), even under conditions of complete nutrient starvation. We mapped this activation to the hyperphosphorylated/acidic domain in the C-terminal tail of SFV non-structural protein nsP3. Viruses with a deletion of this domain (SFV-Δ50), but not other regions in nsP3, displayed a clearly delayed and reduced capacity of Akt stimulation. Ectopic expression of nsP3-wildtype, but not -Δ50, equipped with a membrane anchor was sufficient to activate Akt. We linked PI3K–Akt– mTOR stimulation to the intracellular dynamics of viral replication complexes, which are formed at the plasma membrane and subsequently internalised in a process blocked by the PI3K inhibitor Wortmannin. Replication complex internalisation was observed upon infection of cells with SFV-wt and SFV mutants with deletions in nsP3, but not with SFV34 Δ50, where replication complexes were typically accumulated at the cell periphery. In cells infected with the closely related chikungunya virus (CHIKV), the PI3K–Akt–mTOR pathway was only moderately activated. Replication complexes of CHIKV were predominantly located at the cell periphery. Exchanging the hypervariable C-terminal tail of nsP3 between SFV and CHIKV induced the phenotype of strong PI3K–Akt–mTOR activation and replication complex internalisation in CHIKV. In conclusion, infection with SFV but not CHIKV boosts PI3K–Akt–mTOR through the hyperphosphorylated/acidic domain of nsP3 to drive replication complex internalisation.