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The essential neuroanatomical structure of language processing remains unclear. Here we show in a cohort of 79 consecutive glioma patients undergoing surgery in the dominant hemisphere that postoperative language deficits result from subcortical damage to individualized ROIs within normative white matter tracts. We integrate these findings into a data-driven, non-invasive brain mapping approach capable of using cortical transcranial magnetic stimulation (TMS) mappings and diffusion imaging to localize language-essential regions and predict the long-term functional outcome of personalized surgical strategies with an accuracy of 94%. We use this technique to create a group-level probabilistic atlas of functional white matter in glioma patients, revealing evidence for a novel, disease-specific pattern of subcortical connectivity deep to the temporo-parietal-occipital (TPO) junction that anatomically correlates with regional vulnerability to aphasic damage. This study provides novel insight into the functional anatomy of language processing while defining a reproducible approach for non-invasively mapping essential language function.