Nucleosomes are assembled and disassembled in a highly regulated manner by histone chaperones, which shield histones from non-specific interactions (Hammond, Strømme et al. 2017). From biosynthesis to deposition histones are handed through a cascade of histone chaperones, yet it remains unclear how cells control histone transfer reactions and cleanup spurious interactions. We identified DNAJC9 as a novel histone chaperone that directs protein folding machinery to histone substrates, promoting their entry/re-entry into the supply chain and release from trapped intermediates. DNAJC9 recruits HSP70 catalysis to its histone H3–H4 cargo via its conserved J domain. We elucidate the structure of DNAJC9 in a histone H3–H4 co-chaperone complex with MCM2, revealing how the dual histone and heat shock co-chaperone binds histone substrates. Failure to engage DNAJC9 causes histones to accumulate upstream in the histone supply chain prior to H3–H4 heterodimer formation. In addition, DNAJC9 mutations that abolish HSP70 mediated catalysis traps histones with DNAJC9 shortly after histone biosynthesis and during replication- and transcription-coupled nucleosome assembly. Together, DNAJC9 combines both histone and heat shock co-chaperone abilities to direct HSP70 catalysis towards histone substrates facilitating their supply to and transactions within chromatin.