Circadian rhythm, the “body clock”, plays central roles in diverse facets of physiology. Sleep is crucial for memory consolidation, a notion supported by the fact that structural and functional changes of the neuronal synapses occur during sleep. Thus, we hypothesised that circadian rhythm regulates the synaptic protein N-glycosylation and that alterations of the synaptic N-glycome, in turn, may impact the synapse modulation. As a first step to test this hypothesis, the N-glycome and the underpinning N-glycosylation enzymes of neuronal synaptosomes of mice brains isolated during the light (n = 5, “sleep”) and dark phase (n = 4, “awake”) were investigated using quantitative LC-MS/MS-based glycomics and proteomics. The synaptosomes were density-separated, their purity verified using synaptic protein markers and their membrane protein extracts obtained. In accordance with previous literature, glycomics identified 56 biosynthetically-related, mostly asialylated structures displaying prominent core fucosylation and GlcNAc- or mannose-capped and Lewis-type epitopes. Surprisingly few sleep-wake cycle N-glycome differences were observed within the detailed synaptic N-glycome map. Label-free proteomics confidently identified and quantified 193 glyco-enzymes in the synaptosomes of which 42 glycosyltransferases and glycosidases were found to be involved in N-glycoprotein biosynthesis. Importantly, circadian regulation of known clock proteins (e.g. BMAL1, PER1) was observed, which verified the experimental design and the proteomics data. Interestingly, approximately half of the N-glyco-enzymes including both the catabolic hydrolases and anabolic glycosyltransferases were significantly regulated during sleep, indicating that these are not rate-limiting in the N-glycoprotein biosynthesis. In summary, our data indicate that the neuronal protein N-glycosylation machinery but not the resulting synaptosomal N-glycome fluctuates with circadian rhythm. This study also provides a high-resolution quantitative map of the murine synaptic N-glycome useful for future glycobiological explorations.