The evolutionarily conserved HIRA/Hir histone chaperone complex and ASF1a/Asf1 co-chaperone cooperate to deposit histone (H3/H4)2 tetramers into nucleosomes for replication- independent chromatin assembly. The molecular architecture of the HIRA/Hir complex and its mode of histone deposition has remained unknown since its initial identification nearly three decades ago. Here we report the cryo-EM structure of the S. cerevisiae Hir complex with Asf1/H3/H4 at 2.9–6.8 Å resolution, together with crosslinking mass spectrometry, yeast genetic, and biochemical analyses. We find that the Hir complex forms an arc-shaped dimer with a Hir1/Hir2/Hir3/Hpc2 stoichiometry of 2/4/2/4 with a central cavity in which two copies of Hpc2 from each sub-complex within the dimer are in suitable position to accommodate a histone (H3-H4)2 tetramer. The core of the complex contains Hir1/Hir2/Hir2 trimers and N- terminal segments of Hir3, while C-terminal segments of Hir3 harbor nucleic acid binding properties implicated for double-stranded DNA engagement within the cavity for histone deposition. Despite the near two-fold symmetric scaffold, the structure reveals only one bound Asf1/H3/H4 complex in the cavity, with another presumed Asf1/H3/H4 complex poised outside of the cavity, suggesting a synergetic mechanism for HIRA/Hir-mediated histone deposition in which the Hpc2-assisted energetically unfavorable (H3/H4)2 tetramer can be immediately wrapped by DNA positioned by Hir3.