Neurons canonically communicate through chemical synapses whose structure is formed, refined, and maintained through the coordination of pre- and post-synaptic scaffolding molecules that interact across the synaptic cleft. One such trans-synaptic molecule, Dystroglycan (Dag1), is expressed throughout the body where it is important for muscle integrity, neuronal migration, regulation of the blood-brain barrier, axon targeting, and, as we have recently come to appreciate, the formation of inhibitory synapses. Dystroglycan is composed of two subunits: an extracellular alpha subunit and a transmembrane beta subunit. α-Dystroglycan is extensively glycosylated through the coordination of at least 19 different genes. Mutations resulting in hypoglycosylation lead to dystroglycanopathy, a class of muscular dystrophy characterized by muscular and neurological defects. Dystroglycan localizes to inhibitory synaptic populations throughout the brain, and in this dissertation I explore the mechanism through which Dystroglycan acts at inhibitory hippocampal CCK+/CB1R+ basket synapses (CCK:PyN) and cerebellar molecular layer interneuron synapses onto Purkinje cells (MLI:PC). In Chapter 2, I show that Dystroglycan is required for CCK:PyN axon targeting, synapse formation, and synapse function. This is dependent on Dystroglycan glycosylation, however, mild defects in Dystroglycan glycosylation does not affect synapse function. The Dystroglycan intracellular domain is required for the function, but not formation of CCK:PyN synapses. Furthermore, I show that loss of either extracellular glycosylation or the intracellular domain of Dystroglycan results in increased seizure susceptibility. In Chapter 3 I characterize a suite of Cre driver lines for conditional genetic deletion in cerebellar Purkinje cells, which allow me to dissect Dystroglycan’s synaptic function at different stages of development. In Chapter 4, I show that Dystroglycan is required for MLI:PC synapse formation, function, and maintenance. Glycosylation is required for MLI:PC synapse formation and function while the intracellular domain is required for synapse function but not formation. In Chapter 5 I use an unbiased proteomics screen to identify novel interacting partners of Dystroglycan in an effort to understand the composition of Dystroglycan-containing synaptic complexes. Collectively, these results advance our knowledge of the molecular mechanism behind inhibitory synapse development, and will inform targeted treatments for synaptic defects in dystroglycanopathy.