The mitochondrial (mt) translation release factor (Mrf1) promotes peptidyl-tRNA hydrolysis (PTH) in a codon-specific manner and has been shown to be essential in procyclic T. brucei. However, we demonstrate that cultured bloodstream forms (BF) can tolerate the elimination of this protein by adapting their mt bioenergenetics and employing the codon-independent PTH factor, ICT1. Specifically, BF Mrf1 double knock-out (DKO) cells have less assembled F_oF₁-ATP synthase (complex V) monomers and oligomers, suggesting that the impairment to translation termination results in the depletion of functional A6, a mt encoded subunit of this enzymatic complex. This correlates with a decrease in the mt membrane potential (∆ψ_m), which contributes to the slower growth rate observed in these cells. To compensate for the diminished capacity of complex V to pump protons, the activity and expression levels of the ADP/ATP carrier increase to supplement the ∆ψ_m by the electrogenic exchange of its substrates. Since the cells also became hypersensitive to oligomycin, an inhibitor of the proton pore created by A6, we analyzed if ICT1 could rescue stalled ribosomes. Indeed, while there is no growth phenotype when ICT1 is depleted in wildtype cells, ICT1 silencing in the Mrf1 DKO cell lines severely inhibits growth. Furthermore, the overexpression of ICT1 in the Mrf1 DKO cell lines partially alleviates the observed phenotypes. These outcomes highlight the ability of the BF mitochondrion to adapt when primarily A6 translation is required for the reduced organellar role during this developmental stage.