SignificanceAstrocytic physiological dysfunction contributes to development of the neurodegenerative phenotype in Huntington’s disease (HD), but the structural correlates to this dysfunction are unclear. Here, we used a combination of viral tracing, phenotype-specific tagging, and ultrastructural modalities to reconstruct HD synapses at the nanometer scale in the neostriata of HD mice. We discovered significant impairment in the astroglial engagement of mature striatal synapses. In light of the known deficiencies in glutamate and potassium uptake by HD astrocytes, these findings suggest the potential for leakage of excitatory synaptic contents during neurotransmission, and hence a structural basis for neuronal hyperexcitability in HD. More broadly, our data suggest that astrocytic structural pathology may causally contribute to those neurodegenerative disorders associated with central hyperexcitability.