Correct mitochondrial distribution is critical for satisfying local energy demands and calcium buffering requirements and supporting key cellular processes. The mitochondrially targeted proteins Miro1 and Miro2 are important components of the mitochondrial transport machinery, but their specific roles in neuronal development, maintenance, and survival remain poorly understood. Using mouse knockout strategies, we demonstrate that Miro1, as opposed to Miro2, is the primary regulator of mitochondrial transport in both axons and dendrites. Miro1 deletion leads to depletion of mitochondria from distal dendrites but not axons, accompanied by a marked reduction in dendritic complexity. Disrupting postnatal mitochondrial distribution in vivo by deleting Miro1 in mature neurons causes a progressive loss of distal dendrites and compromises neuronal survival. Thus, the local availability of mitochondrial mass is critical for generating and sustaining dendritic arbors, and disruption of mitochondrial distribution in mature neurons is associated with neurodegeneration. Display omitted •Miro1 deletion alters mitochondrial distribution in dendrites but not axons•Mitochondrial distribution impacts dendritic development•Correct mitochondrial distribution is key to maintain complex dendritic geometries•Aberrant dendritic mitochondrial distribution triggers neurodegeneration Complex dendritic morphologies are essential for neural circuit formation and brain computation. López-Doménech et al. demonstrate that Miro1-dependent dendritic mitochondrial positioning critically regulates the development of the dendritic tree and sustains arborization. Disrupting mitochondrial distribution in mature neurons leads to the loss of dendritic complexity, which precedes neurodegeneration.