The molecular mechanism of lipoprotein binding by the low‐density lipoprotein (LDL) receptor (LDLR) is poorly understood, one reason being that structures of lipoprotein–receptor complexes are not available. LDLR uses calcium‐binding repeats (LRs) to interact with apolipoprotein B and apolipoprotein E (ApoB and ApoE). We have used NMR and SPR to characterize the complexes formed by LR5 and three peptides encompassing the putative binding regions of ApoB (site A and site B) and ApoE. The three peptides bind at the hydrophilic convex face of LR5, forming complexes that are weakened at low [Ca2+] and low pH. Thus, endosomal conditions favour dissociation of LDLR/lipoprotein complexes regardless of whether active displacement of bound lipoproteins by the β‐propeller in LDLR takes place. The multiple ApoE copies in β very low density lipoproteins (β‐VLDLs), and the presence of two competent binding sites (A and B) in LDLs, suggest that LDLR chelates lipoproteins and enhances complex affinity by using more than one LR.