We recently discovered an immune-related class of glycoproteins decorated with paucimannosidic N-glycans (PMGs) [Man(M)1-3GlcNAc2Fuc(F)0-1] expressed by innate immune cells [Thaysen-Andersen et al., J Biol Chem, 290(14):8789, 2015]. Herein, we extend these findings by investigating a possible association between protein paucimannosylation and cancer. To this end, the distribution of PMGs released from proteins expressed by a wide range of human cancer cells and tissues and matching non-cancerous specimens were determined by re-interrogating a large collection of published and unpublished N-glycomics datasets acquired over a decade within our laboratories using a uniform porous graphitised carbon liquid chromatography tandem mass spectrometry method. The total level of PMGs within the entire N-glycome and the relative distribution of the individual PMG species (M1, M1F, M2, M2F, M3, and M3F) were accurately determined using this well-established quantitative glycomics platform. In total, N-glycome profiling data from 34 different cancer cell lines, and 133 tissue samples spanning 11 cancer types with matching non-cancerous specimens, were (re-) curated from 467 datasets. Although the total PMG levels varied dramatically across and within the investigated cancer types (1.0%-50.2%), particularly the α1,6-fucosylated bi- and tri-mannosylated N-glycans (M2F and M3F) were consistently prominent features of most of the cancer cell lines. Analyses of paired (tumour/non-tumour) and stage-stratified tissues demonstrated that PMGs are significantly enriched in tumours from several cancer types including non-melanoma skin cancer (p = 0.0145), liver (p = 0.0033) and colorectal (p = 0.0017) cancers and are increased with prostate cancer and chronic lymphocytic leukaemia progression (both p < 0.02). Based on these correlation-type observations we conclude that protein paucimannosylation represents a significant, but non-uniform, glycoepitope of human cancers. These findings advance our understanding of the glyco-features expressed by human cancers and encourage further cause-effect type studies of paucimannosylation in cancer tumorigenesis and metastasis.