Platelet activation induces the secretion of proteins that promote platelet aggregation and inflammation. Here we detail the most sensitive analysis to date of the platelet secreted proteome with the detection of >1,300 proteins. Unbiased scanning for post-translational modifications within platelet secreted proteins highlighted O-glycosylation as being a major component. For the first time, we detected high stoichiometry O-fucosylation on previously uncharacterised sites including multimerin-1 (MMRN1), a major alpha granule protein that supports platelet adhesion to collagen and is a carrier for platelet factor V. The N-terminal elastin microfibril interface (EMI) domain of MMRN1, a key site for protein-protein interaction, was O-fucosylated at a conserved threonine (T216) with high stoichiometry. Secretion was inhibited of a MMRN1 T216A mutant that could not be O-fucosylated on the EMI domain, supporting a functional role of EMI domain O-fucosylation in protein quality control. Data from interaction predictions using Alphafold2-Multimer suggested that two widely expressed fucosyltransferases of unknown function, FUT10 and FUT11, were responsible for this modification. Co-immunoprecipitation assays, in vitro O-fucosylation assays and knockout cell lines demonstrated FUT10/11 is necessary and sufficient for EMI domain O-fucosylation. Using crosslinking mass spectrometry on purified proteins, we have validated the very high-quality predicted structure from Alphafold2 for the FUT10/FUT11 interaction with the EMI domain. The EMI domain is present in 18 distinct mammalian proteins that are either secreted, or cell surface integral membrane proteins and produced by a diverse array of tissues such as platelets, neurons and muscle. We have confirmed using electron activated dissociation (EAD) that the EMI domain of 4 other proteins, EMILIN1, EMID1, MMRN2 and COL26A1 were also O-fucosylated in their EMI domain. This suggests the widespread necessity of this new modification for protein function. Future work will focus on characterisation of platelet phenotypes in FUT10/11 double knock-out mice.