Post-translational modifications (PTMs) greatly expand the function and potential for regulation of protein activity, and O-glycosylation is among the most abundant and diverse PTMs. Initiation of O-GalNAc glycosylation is regulated by 20 distinct GalNAc-transferases (GalNAc-Ts), and deficiencies in individual GalNAc-Ts are associated with human disease, causing subtle but distinct phenotypes in model organisms. Here, we generated a set of isogenic keratinocyte cell lines with and without the three dominant and differentially expressed GalNAc-Ts. Through the ability of keratinocytes to form epithelia, we investigated the phenotypic consequences of the loss of individual GalNAc-Ts. We also used isogenic keratinocyte cell lines to probe cellular responses to the ablation of GalNAc-Ts through global transcriptomic, differential glycoproteomic, and differential phosphoproteomic analyses. We demonstrate that loss of individual GalNAc-T isoforms causes distinct epithelial phenotypes through their effect on distinct biological pathways; GalNAc-T1 targets are associated with components of the endomembrane system, GalNAc-T2 targets – with cell-ECM adhesion, and GalNAc-T3 targets – with epithelial differentiation. Thus, GalNAc-T isoforms serve specific roles during human epithelial tissue formation.