Cellular lipids presented by human CD1 proteins are controlling elements for the development and response of lipid-reactive T cells in homeostasis, inflammation, and microbial infections. Whereas most CD1 studies focused on a few named lipids that lead to T cell activation or deactivation, the scope and nature of self lipids acquired by four human CD1 molecules have not been characterized. We adapted a comparative lipidomic platform to profile the cellular lipids bound to recombinant human CD1a, CD1b, CD1c, or CD1d proteins during their egress through the secretory pathway in two cell types. The broadly separating liquid chromatography combined with sensitive time-of-flight mass spectrometry allows the enumeration and identification of bound lipid types with unique molecular features, defined as one linked retention time-mass-intensity value. This unbiased profiling approach supports four general conclusions about CD1 antigen display. First, human CD1 proteins broadly survey cellular lipids through the capture of more than 1000 molecularly distinct glycolipids, phospholipids, lysolipids, ether-linked lipids, or sphingolipids. Second, despite marked differences in the number, size, and architecture of CD1 pockets, human CD1 proteins capture an overlapping profile of lipids. Eighty percent of CD1-associated lipids were detected from multiple CD1 proteins. Third, CD1b and CD1c with larger groove volume released phosphatidylcholine and sphingomyelin with shorter alkyl chains in comparison to the groove size and overlapping lipid association of CD1d molecule, supporting a regulatory role of spacer lipids in rendering CD1b antigen presentation. Fourth, collision-induced dissociation mass spectrometry identified more than ten families of overlapping cellular lipids, including lipid families capable of activating or blocking T cell responses.  These data, along with a broader listing of the mass values of overlapping CD1-associated lipids, support a conserve manner of CD1 binding of self lipids and provide a resource to identify self antigens or non-permissive ligands for T cell response.