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The wide variation in muscle fibre type distribution across individuals, along with the very different energy consumption rates in slow versus fast muscle fibres, suggests that muscle fibre typology contributes to inter‐individual differences in metabolic rate during exercise. However, this has been hard to demonstrate due to the gap between a single muscle fibre and full‐body exercises. We investigated the isolated effect of triceps surae muscle contraction velocity on whole‐body metabolic rate during cyclic contractions in individuals a priori selected for their predominantly slow (n = 11) or fast (n = 10) muscle fibre typology by means of proton magnetic resonance spectroscopy (1H‐MRS). Subsequently, we examined their whole‐body metabolic rate during walking and running at 2 m/s, exercises with comparable metabolic rates but distinct triceps surae muscle force and velocity demands (walking: low force, high velocity; running: high force, low velocity). Increasing triceps surae contraction velocity during cyclic contractions elevated net whole‐body metabolic rate for both typology groups. However, the slow group consumed substantially less net metabolic energy at the slowest contraction velocity, but the metabolic difference between groups diminished at faster velocities. Consistent with the more economic force production during slow contractions, the slow group exhibited lower metabolic rates than the fast group while running, whereas metabolic rates were similar during walking. These findings provide important insights into the influence of muscle fibre typology on whole‐body metabolic rate and emphasize the importance of considering muscle mechanical demands to understand muscle fibre typology related differences in whole‐body metabolic rates. Key points: Muscle fibre typology is often suggested to affect whole‐body metabolic rate, yet convincing in vivo evidence is lacking.Using isolated plantar flexor muscle contractions in individuals a priori selected for their predominantly slow or fast muscle fibre typology, we demonstrated that having predominantly slow muscle fibres provides a metabolic advantage during slow muscle contractions, but this benefit disappeared at faster contractions.We extended these results to full‐body exercises, where we demonstrated that higher proportions of slow fibres associated with better economy during running but not when walking.These findings provide important insights into the influence of muscle fibre typology on whole‐body metabolic rate and emphasize the importance of considering muscle mechanical demands to understand muscle fibre typology related differences in whole‐body metabolic rate. [ABSTRACT FROM AUTHOR]