Direct cortical stimulation (DCS) is the clinical gold standard for identifying functional cortex in the human brain, which is essential for the safe removal of brain lesions. Defining the electro-physiological properties of DCS-positive cortical regions may facilitate the identification of critical language regions, thereby permitting safe glioma resections in communities without access. Leveraging a multicenter electrophysiologic dataset of DCS-positive language regions spatially matched with subdural arrays, we analyzed regions identified as functionally critical (DCS+) versus functionally non-critical (DCS-) during intraoperative language mapping. In IDH-mutant gliomas, DCS+ regions exhibited significantly greater speech-related neural activity and enhanced encoding and decoding of linguistic and semantic features. We demonstrate that resting-state classifiers distinguish DCS+ from DCS- regions in IDH-mutant tumors. Task-based and resting-state electrophysiologic distinctions were pathology-specific and not present in IDH-wildtype glioblastomas. These findings may accelerate DCS mapping by guiding surgeons to priority regions, improving efficiency, and patient outcomes.