Brassinosteroids (BRs), the plant steroid hormones, play an important role in mediating plant responses to developmental and environmental cues. BRs signal through a membrane receptor BRI1 and a GSK3 kinase BIN2 to control the activity of BES1/BZR1 family transcription factors. To understand how BES1 regulates gene expression, I looked into both trans-acting protein factors and cis-acting DNA elements that affect BES1 functions, by yeast genetic screen and chromatin immunoprecipitation coupled with DNA microarray (ChIP-chip), respectively. We identified 1609 BES1 direct target genes and discovered conserved DNA motifs in BES1 binding regions. We also showed that BES1 target genes were largely devoid of H3K27me3. In contrast, 35% of BES1 target genes were associated with H3K9me3 and two putative H3K9me3 demethylases, ELF6 and REF6, were recruited to target gene promoters by interacting with BES1, loss-of-function of which caused BR-related phenotypes. Therefore, we provided significant insights into mechanisms of BES1-regulated gene expression.