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Abstract Elemental sulfur (S₈⁰)‐oxidising Sulfolobales (Archaea) dominate high‐temperature acidic hot springs (>80°C, pH <4). However, genomic analyses of S₈⁰‐oxidising members of the Sulfolobales reveal a patchy distribution of genes encoding sulfur oxygenase reductase (SOR), an S₈⁰disproportionating enzyme attributed to S₈⁰oxidation. Here, we report the S₈⁰‐dependent growth of two Sulfolobales strains previously isolated from acidic hot springs in Yellowstone National Park, one of which associated with bulk S₈⁰during growth and one that did not. The genomes of each strain encoded different sulfur metabolism enzymes, with only one encoding SOR. Dialysis membrane experiments showed that direct contact is not required for S₈⁰oxidation in the SOR‐encoding strain. This is attributed to the generation of hydrogen sulfide (H₂S) from S₈⁰disproportionation that can diffuse out of the cell to solubilise bulk S₈⁰to form soluble polysulfides (S_x²⁻) and/or S₈⁰nanoparticles that readily diffuse across dialysis membranes. The Sulfolobales strain lacking SOR required direct contact to oxidise S₈⁰, which could be overcome by the addition of H₂S. High concentrations of S₈⁰inhibited the growth of both strains. These results implicate alternative strategies to acquire and metabolise sulfur in Sulfolobales and have implications for their distribution and ecology in their hot spring habitats.