Type 1 conventional dendritic cells (cDC1s) are uniquely specialized to cross-present exogenous, cell-associated antigens to initiate cytotoxic  T cell immunity against tumors and viruses. While this process strictly requires the multi-domain BEACH protein WDFY4, the underlying molecular mechanism and spatial parameters governing its function have remained undefined. Using proximity-dependent proteomics, reversible in situ cross-linking mass spectrometry and structural modeling in primary cDC1s, we identified the evolutionarily conserved VAC14-PIKFYVE-FIG4 lipid kinase complex as a primary interactor of WDFY4. We demonstrate that VAC14 binds directly to the -terminal PH-BEACH-WD40 domains of WDFY4, while PIKFYVE and FIG4 associate indirectly. These findings suggest that WDFY4 might drive localized phosphatidylinositol 3,5-bisphosphate () synthesis on antigen containing endosomes. High-resolution super-resolution imaging in primary cells revealed that under homeostatic conditions, WDFY4 resides on a juxtanuclear tubulovesicular network co-localizing with Rab43. This network is adjacent to a characteristic large intracellular store of MHC class I molecules. Previous models suggested this pool to reside within a canonical  endocytic recycling compartment (ERC), but we find these compartments to be clearly distinct, as a single-paralog-specific Rab11a monoclonal antibody clearly segregated the ERC from intracellular MHC class I. Upon pathogen/antigen capture, the WDFY4/Rab43/MHC-I complex merges with pathogen containing endosomes, suggesting a framework for a vesicular route of WDFY4-dependent cross-presentation.