Recent discoveries in the field of immunometabolism have emphasised the importance of mitochondria in the context of T cell development, differentiation, signalling and exhaustion. However, the question of whether mitochondria can actively participate to the killing activity of differentiated, cytotoxic CD8+ T cells (CTLs) remains unanswered. In this work I analyse CTLs derived from USP30-deficient mice, which have been previously characterised as part of the Infection, Immunity and Immunophenotype Consortium and shown to display altered CTL killing. USP30 is a deubiquitinase localised on the outer mitochondrial membrane and on the peroxisomal membrane, where it counteracts mitophagy and pexophagy by cleaving ubiquitin chains from target proteins. Here I characterise T cell motility, signalling, energy requirements and cytotoxicity in CD8+ T cells derived from splenocytes of Usp30-/- mice. Furthermore, I test different mitochondrial functions using both genetic and pharmacological manipulation of oxidative phosphorylation, mitochondrial calcium flux and mitochondrial translation. I highlight mitochondrial translation as a previously uncharacterised mitochondrial function that allows for optimal CTL cytotoxicity. Specifically, I show that both Usp30-/- CTLs and CTLs in which mitochondrial translation is inhibited display impaired cytosolic protein synthesis, which results in lower abundance of cytolytic molecules essential for killing. This requirement was especially evident when CTLs were limiting in numbers or when they needed to sustain killing for prolonged time, underscoring the importance of efficient mitochondrial translation during an immune challenge. Finally, I investigate mechanisms that could link mitochondrial translation to a loss of cytosolic protein synthesis, including mTOR signalling, mitochondrial reactive oxygen species generation and the integrated stress response. Overall, this work uncovers a novel role for mitochondrial translation in CTL cytotoxicity and adds to the growing body of evidence revealing the multifaceted and crucial roles of mitochondria in T cell function.