The immunopeptidome comprises the suite of human leukocyte antigen (HLA)-bound peptides that are presented at the cell surface for recognition by patrolling T cells. A variety of post-translationally modified peptides have been shown to be presented by HLA molecules, emphasising the importance of the antigen processing pathway in continuously monitoring intracellular protein states. However, little is known about the nature or extent to which glycosylated peptides might represent a yet-to-be-explored component of the immunopeptidome, in part due to technical challenges for direct characterisation of sequence and glycan. We developed an algorithm that facilitates the in silico enrichment and bespoke analysis of oxonium ion-containing spectra. We demonstrate this novel strategy to rapidly profile the immunoglycopeptidome, revealing that glycopeptides occupy between 0.5-10% of HLA-bound peptides. We further show this proportion is dependent upon cell type and HLA allele and that the glycan composition is largely what appears to be short O-linked glycans (e.g. HexNAcHexNeuAc(2)) but also includes N-linked paucimannose such as HexNAc(2)Hex(3)Fuc(1). Additionally, scanning for sufficiently matching pairs of oxonium ion-negative and positive spectra (whose precursor masses differ by that of any glycan observed within the dataset) provides the first evidence that both glycosylated and non-/de-glycosylated peptides are simultaneously presented by the immune system. Collectively, these data provide the most comprehensive assessment of the immunoglycopeptidome to date, emphasising the predominance of O-linked glycosylated peptides and reveals another important facet of immune surveillance of glycosylated antigens.