Living biological systems display a fascinating ability to self-organise their metabolism. This ability ultimately determines metabolic robustness that is fundamental to control cellular behaviour. However, fluctuations in metabolism can affect cellular homeostasis through transient oscillations. For example, yeast cultures exhibit rhythmic oscillatory behaviour in high-cell density continuous cultures. Oscillatory behaviour provides a unique opportunity for quantitating the robustness of metabolism, as cells respond to changes by inherently compromising metabolic efficiency. Here, we quantify the limits of metabolic robustness in self-oscillating autotrophic continuous cultures of the gas-fermenting acetogen Clostridium autoethanogenum. On-line gas analysis and high-resolution temporal metabolomics showed oscillations in gas uptake rates and extracellular by-products synchronised with biomass levels. Loss of H2 uptake makes CO the sole carbon and energy source until cells recover uptake of H2 in synchrony with increasing biomass levels. Intriguingly, oscillations are not linked to translational control as no differences were observed in protein expression during oscillations. However, intracellular metabolomics analysis revealed decreasing levels of redox ratios in perfect synchrony with the cycles. Therefore, we developed a thermodynamic metabolic flux analysis (tMFA) model to investigate if regulation in acetogens is controlled at the thermodynamic level. The data shows that the feasible range for the thermodynamic driving force of the Nfn transhydrogenase complex (i.e. NADH/NAD+×NADP+/NADPH) closely matched the experimentally observed range. The data indicate that metabolic oscillations in gas fermentation acetogens are controlled at the thermodynamic level. Our work suggests thermodynamic control of metabolism, potentially contributing to metabolic efficiency and working as a mean of energy conservation.