Membrane trafficking defects are one of the core components of Parkinson’s Disease (PD), a progressive neurodegenerative disorder that results in severe motor deficits. Several genes associated with Clathrin-Mediated Endocytosis (CME) have been identified as PD risk genes, suggesting a putative link between trafficking defects and early nigrostriatal dysfunction. Intriguingly, recent work on endocytosis-defective mutants has implicated a renowned PD protein: Parkin (or PARK2), an E3 Ubiquitin ligase conventionally involved in mitochondrial quality control, in CME. Parkin is reported to mono-ubiquitinate Synaptic Vesicle Endocytosis (SVE) proteins such as EndophilinA1, Synaptojanin1 (SJ1) and Dynamin1, indicating that it may regulate their activity. Additionally, Parkinsonism linked SJ1RQ-KI as well as EndophilinA1-KO mice show increased levels of Parkin compared to other PD proteins. Hence, we propose that Parkin has a novel role in modulating SVE through regulation of CME protein-protein interactions. Utilizing Parkin-KO/SJ1RQ-KI mice, we investigated the interaction between these proteins at a functional level. We observe decreased survival rate in double mutant mice alongside increase in epileptic seizures and behavioral defects. Aberrant clustering of SVE proteins is observed in synapses, hinting at elevated synaptic dysfunction in Parkin-KO/SJ1RQ-KI mice compared to reported defects in SJ1RQ-KI mice while Parkin-KO and WT mice have no defects. Despite Parkin’s neuroprotective capacity, it is crucial to elucidate its exact physiological function in neurons as it is ubiquitously expressed. The present study contributes to our understanding of early synaptic defects in PD and Parkin’s non-canonical functions, potentially allowing us to target Parkin for future therapeutic strategies.