O-Fucosylation plays crucial roles in various essential biological events. Alongside the well-established O-fucosylation of Epidermal Growth Factor-like (EGF) repeats by Protein O-fucosyltransferase 1 (POFUT1) and Thrombospondin Type 1 Repeats (TSRs) by POFUT2, we recently identified a novel type of O-fucosylation on Elastin Microfibril Interface (EMI) domains of Multimerin-1 (MMRN1). Here, using Alphafold2 screens, co-immunoprecipitation, enzymatic assays combined with mass spectrometric analysis, and CRISPR-Cas9 knockouts, we demonstrate that FUT10 and FUT11, originally annotated in UniProt as α1-3 fucosyltransferases, are actually POFUTs responsible for modifying EMI domains; thus, we renamed them as POFUT3 and POFUT4, respectively. Like POFUT1/2, POFUT3/4 function in the endoplasmic reticulum (ER), require folded domain structures for modification, and participate in a non-canonical ER quality control pathway for EMI domain-containing protein secretion. This finding expands the O-fucosylation repertoire and provides an entry point for further exploration in this emerging field of O-fucosylation.