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The operating length ranges of mammalian jaw muscles have been estimated using twitch contractions or force measurements at the bite point, prompting a consensus that jaw muscles operate at short lengths on their force-length (FL) curve. However, since activation intensity truncates muscle optimal length ( L O ), we hypothesized that L O of rat superficial masseter (SM) would decrease with activation intensity, with high-force biting involving muscle shortening from long lengths on the FL curve. We measured muscle activation, strain, and force in vivo during biting on food with varying hardness and mapped the in vivo data from each muscle ( N  = 6) onto its FL relationship, measured in situ . Submaximal L O was approx. 12% shorter than twitch L O , and SM bite forces averaged 4.1 ± 3.9 N/cm 2 (mean ± S.D.) and reached 10.6 N/cm 2 , corresponding to muscle activation and food hardness. Length operation ranged from 7% below L O (ascending FL plateau), to 27% beyond (descending limb). The finding that jaw muscles operate at long, potentially unstable lengths, particularly during hard food biting significantly expands our understanding of skeletal muscle function, with broad implications for craniofacial evolution, muscle mechanics and control, and healthy as well as pathological function of the jaw musculoskeletal system.