In peripheral tissues, cDC1s encounter a complex mixture of inflammatory and tolerogenic antigens, including self-derived antigens as well as commensal and pathogenic microbial antigens. In the vacuolar pathway of cross-presentation, endosomal maturation enables the generation of peptides for MHCI-loading, and studies indicate cargo-derived pattern recognition receptor signaling directs endosomal processing for cross-presentation. Thus, antigen identity can shape downstream processing and tailor immune responses to the tissue. Tumor microenvironments are antigenically heterogeneous and include host and microbial derived antigen sources, yet how cDC1s integrate simultaneous inputs from tumor and non-tumor antigens at the single-cell level is unclear. Using tissue- and tumor-derived fluorescent antigen tracking combined with endosome phenotyping, we imaged distinct antigen sources within single cDC1s from tumors. We find that cDC1s concurrently internalize multiple antigens, sorting them into source-biased endosomal compartments. Tumor-derived cargo significantly colocalizes with tolerogenic self and microbial antigen sources compared to pathogen-derived antigen, and we find that endosomal maturation is dependent on cargo identity. In tumor+self+ cDC1s, the majority of tumor antigen colocalizes with self-antigen while only a small proportion of endosomes harbor tumor alone (tumor+). Interestingly, in these cDC1s, MHCI preferentially associates with tumor+self+ compared to tumor+ endosomes suggesting dual-antigen loaded endosomal cargo may be fated for cross-presentation. However, concurrent uptake of self-antigen and tumor antigen significantly reduced tumor-specific CD8+ T cell stimulation compared to cDC1s that only internalized tumor antigen. Conversely, self-antigen specific CD8+ T cell stimulation increased when T cells were stimulated with tumor+self+ cDC1s. Ultimately, we find that cDC1 co-uptake of self- and tumor antigen significantly reduces the quantity of tumor peptide loaded MHCI on the cell surface suggesting self-derived cargo potentially competes for intraendosomal MHCI-loading. These results identify a mechanism by which tolerizing self-antigens in the tumor microenvironment can subvert cDC1-mediated antitumor immunity and emphasize antigenic context as a determinant of cross-presentation.