Mammals encode a highly conserved family of histone H3 lysine 4 (H3K4) demethylases known as the JARIDs that have important roles in regulating gene expression and controlling the balance between pluripotency and differentiation in stem cells. Gaining mechanistic and physiological insight on the consequences of JARID-mediated H3K4 demethylation has been challenging due the high level of redundancy in the mammalian JARID gene family. Methylated histones function as scaffolds for the recruitment of activating or repressive chromatin factors. The recruitment of specific factors is likely modulated by JARID-mediated H3K4 demethylation. We study Jhd2, the single JARID family H3K4 demethylase, in budding yeast Saccharomyces cerevisiae, using this simple model to investigate the consequences of JARID-mediated H3K4 demethylation. Genetic interrogation of JHD2 revealed that temperature sensitive growth defects exhibited by mutants of the highly conserved histone chaperones Spt6 and FACT are rescued by JHD2 deletion. Rescue is specific to loss of JHD2 enzymatic activity and requires H3K4 trimethylation. JHD2 deletion does not directly affect FACT protein stability or genomic localization, but genetic epistasis suggests that JHD2 deletion rescues Spt6 and FACT temperature sensitivity indirectly through the modulation of the small Rpd3 histone deacetylase complex. In our working model, Jhd2-mediated H3K4 demethylation functions to regulate Rpd3S recruitment through its plant homeodomain containing subunit Rco1.