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Failed regeneration of CNS myelin contributes to clinical decline in neuroinflammatory and neurodegenerative diseases, for which there is an unmet therapeutic need. Here we reveal that efficient remyelination requires death of proinflammatory microglia followed by repopulation to a pro-regenerative state. We propose that impaired microglia death and/or repopulation may underpin dysregulated microglia activation in neurological diseases, and we reveal therapeutic targets to promote white matter regeneration.Lloyd et al. find that regeneration of CNS myelin requires death of proinflammatory microglia followed by repopulation to a pro-regenerative state, revealing new therapeutic targets for neurodegenerative disease.