Regulation of chromatin and control over the expression of the nuclear genome are essential for normal growth and development across diverse eukaryotic taxa. In the model plant Arabidopsis thaliana, failure to properly regulate chromatin is often met with deleterious consequences such as increased susceptibility to environmental stress. Despite their clear importance, the regulation of chromatin and maintaining the organization of the genome are complex processes and new insights continue to adjust and broaden the view of how these processes occur and how they fundamentally direct developmental programs and plasticity. We have identified a gene, XAP5 CIRCADIAN TIMEKEEPER (XCT), as being essential for normal chromatin regulation in Arabidopsis. This gene was initially identified in a mutant screen looking for plants with altered circadian rhythms. Subsequent analyses revealed that XCT is important for the proper functioning of diverse biological processes, including ethylene and ABA signaling, response to environmental stress, flowering time, and photosynthesis. The apparent global importance of XCT prompted the genome-wide analysis of nuclear DNA methylation and transcriptional patterns in xct mutants, which revealed that XCT is required for both normal DNA methylation in all sequence contexts and in maintaining transcriptional control of diverse loci. The entirety of data posits that XCT is a chromatin-associated protein required for normal growth and development. Given that XCT is a well-conserved protein across eukaryotes, this work provides the foundation for studying chromatin-associated roles of XCT-like proteins in other organisms across eukaryotic kingdoms of life.