Few aerobic hyperthermophiles degrade polysaccharides. Here, we describe the genome-enabled enrichment and optical tweezer-based isolation of an aerobic polysaccharide-degrading hyperthermophile, Fervidibacter sacchari, which was originally ascribed to candidate phylum Fervidibacteria. F. sacchari uses polysaccharides and monosaccharides as sole carbon sources from 65-87.5 °C and expresses 191 carbohydrate-active enzymes (CAZymes) according to RNA-Seq and proteomics, including 30 with unusual glycoside hydrolase (GH)109, 177, or 179 domains. Many CAZymes were also expressed in a proteolytic enrichment culture, and fluorescence in situ hybridization and nanoscale secondary ion mass spectrometry confirmed rapid assimilation of 13C-starch in spring sediments. Purified GHs were optimally active at 80-100 °C on eight different polysaccharides. Finally, we reassign Fervidibacteria as a class within phylum Armatimonadota, along with 18 other species, and trace the evolution of aerobic and anaerobic polysaccharide catabolism within the phylum. This study establishes Fervidibacteria as unique hyperthermophilic polysaccharide-degrading specialists in terrestrial geothermal springs.