Parkinson’s disease (PD) is the second most common age-related neurodegenerative disorder characterized by the formation of cellular inclusions inside neurons that predominantly consist of misfolded α- synuclein (α-syn), leading to neuronal dysfunction. The clearance of α-syn aggregates by microglia, the brain’s resident innate immune cells, has emerged as particularly critical for the progression of PD, given their demonstrated ability to scavenge extracellular α-syn with the highest capacity among all brain cells. Here, we present a novel mechanism of neuron-microglia communication through the formation of tunneling nanotubes (TNTs), which enable the extraction of fibrillar α-syn aggregates from neurons into microglia. Subsequently, microglia donate their healthy mitochondria to burdened neurons to maintain neuronal health thereby normalizing α-syn-induced intraneuronal levels of radical oxygen species and aggregate-induced changes in the neuronal transcriptome. Compromising mitochondrial function by treatment of microglia with the electron transport chain blocker Antimycin A prior to the formation of TNTs completely abolishes these neuroprotective effects. Likewise, α-syn-suppressed neuronal activity is rescued by co-incubation with microglia and formation of TNTs. Aggregate transfer from neurons to microglia through TNTs was reduced in LRRK2 G2019S mutant microglia, suggesting that an impairment of the observed mechanism may partly account for the pathology associated with this gene variant in PD. With this, we describe a novel rescue mechanism by which microglia actively clear neurons of misfolded protein aggregates. Failure of this mechanism is likely to be crucial to disease progression and could have significant consequences for cellular outcomes.