We have previously reported that silencing of galectin‐4 expression in polarized HT‐29 cells perturbed apical biosynthetic trafficking and resulted in a phenotype similar to the inhibitor of glycosylation, 1‐benzyl‐2‐acetamido‐2‐deoxy‐β‐d‐galactopyranoside (GalNAcα‐O‐bn). We now present evidence of a lipid raft‐based galectin‐4‐dependent mechanism of apical delivery of glycoproteins in these cells. First, galectin‐4 recruits the apical glycoproteins in detergent‐resistant membranes (DRMs) because these glycoproteins were depleted in DRMs isolated from galectin‐4‐knockdown (KD) HT‐29 5M12 cells. DRM‐associated glycoproteins were identified as ligands for galectin‐4. Structural analysis showed that DRMs were markedly enriched in a series of complex N‐glycans in comparison to detergent‐soluble membranes. Second, in galectin‐4‐KD cells, the apical glycoproteins still exit the Golgi but accumulated inside the cells, showing that their recruitment within lipid rafts and their apical trafficking required the delivery of galectin‐4 at a post‐Golgi level. This lectin that is synthesized on free cytoplasmic ribosomes is externalized from HT‐29 cells mostly in the apical medium and follows an apical endocytic–recycling pathway that is required for the apical biosynthetic pathway. Together, our data show that the pattern of N‐glycosylation of glycoproteins serves as a recognition signal for endocytosed galectin‐4, which drives the raft‐dependent apical pathway of glycoproteins in enterocyte‐like HT‐29 cells.