The plastid of chlorarachniophytes is distinguished by the retention of a relict nucleus (nucleomorph) derived from a green algal endosymbiont, which is located in the periplastidal compartment (PPC). The nucleomorph genome of a chlorarachniophyte, Bigelowiella natans, encodes several plastid-targeted proteins and hundreds of housekeeping proteins, but it lacks many fundamental genes to maintain itself. Here we report the first two host nucleus-encoded genes for proteins targeted to the nucleomorph, histone H2A and H2B. We identified 20 histone genes from the host nuclear genome, and based on phylogenetic analyses predicted that most of these are derived from the host, but that two histone genes are symbiont-derived. The genes both encode N-terminal extensions resembling PPC targeting signals, further suggesting they function in the nucleomorph. Using green fluorescent protein (GFP) fusion proteins expressed in transformed cells, we confirmed that the putative symbiont H2A and H2B were targeted into the nucleomorph, whereas putative host proteins were localized to the host nucleus. Furthermore, we have developed a method to temporarily synchronize B. natans cells, and confirmed that both host and symbiont histone expression is controlled during the cell cycle. Our findings provide the first evidence of how the nucleomorph may be regulated by host-encoded gene products.