Estrogens affect cerebellar activity and cerebellar-based behaviors. Within the adult rodent cerebellum, the best-characterized action of estradiol is to enhance glutamatergic signaling. However, the mechanism(s) by which estradiol promotes glutamatergic neurotransmission remain unknown. Within the mouse cerebellum, we find that estrogen receptor activation of mGluR1a strongly enhances neurotransmission at the parallel fiber-Purkinje cell synapse. The blockade of local estrogen synthesis within the cerebellum results in a diminution of glutamatergic neurotransmission. Correspondingly, decreased estrogen availability via gonadectomy or blockade of aromatase activity negatively impacts locomotor performance. These data indicate that local- and not just gonadal-derived estrogens affect cerebellar physiology and function. In addition, estrogens were found to facilitate parallel fiber-Purkinje cell synaptic transmission in both sexes. As such, the actions of estradiol to support cerebellar neurotransmission and cerebellar-based behaviors may be fundamental to understanding the normal processing of activity within the cerebellar cortex.