Chromatin organization is essential for coordinated gene expression, genome stability, and inheritance of epigenetic information. Main components of chromatin assembly are specific complexes such as CHROMATIN ASSEMBLY FACTOR 1 (CAF-1) and HISTONE REGULATOR (HIR) that deposit histones in a DNA synthesis-dependent or -independent manner, respectively. Here, we characterize the role of the plant orthologs HISTONE REGULATOR A (HIRA), UBINUCLEIN (UBN) and CAlcineurin BINding protein 1 (CABIN1) constituting the HIR complex. Arabidopsis loss-of-function mutants for the different subunits of the complex are viable but present reduced fertility in case of hira mutants. We show that loss of HIRA reduces extractable histone H3 protein levels and decreases nucleosome occupancy at both actively transcribed genes and heterochromatic regions. Concomitantly, HIRA contributes to silencing maintenance of pericentromeric repeats and certain transposons. A genetic analysis based on crosses between mutants deficient in subunits of the CAF-1 and HIR complexes shows that the simultaneous loss of both, CAF-1 and HIR histone H3 chaperone complexes, impacts plant survival, growth and reproductive development severely. Our results suggest that HIRA partially rescues impaired histone deposition in fas mutants to preserve nucleosome occupancy and imply plasticity in histone variant interaction and deposition. This article is protected by copyright. All rights reserved.