Histone H3 lysine 4 methylation (H3K4me) is enriched at active promoters and promotes the recruitment of chromatin regulators, yet how cells protect H3K4-methylated promoter chromatin from inappropriate remodeling remains unknown. Here, we show that proteins encoded by the essential genes jmj3 and lid2 in fission yeast function coordinately to preserve promoter chromatin stability by limiting inappropriate H3K4me-dependent NuA4 acetyltransferase chromatin engagement. Decreased NuA4 at the chromatin restricts excessive histone H4 acetylation, SWI/SNF-mediated remodeling, and promoter-associated nucleosome-sized fragile particle (NSFP) destabilization, thereby maintaining transcriptional programs that support vegetative growth. Upon nutrient limitation, TOR complex 1 (TORC1) inactivation triggers Ubc14-Dbl4-dependent degradation of Jmj3 and Lid2, which results in programmed promoter remodeling. Moreover, loss of Jmj3/Lid2 couples meiotic transcriptional reprogramming with Rec12-dependent recombination hotspot activation, ensuring efficient meiotic differentiation. Together, our findings identify a nutrient-responsive mechanism that safeguards H3K4-methylated promoter chromatin while permitting regulated chromatin remodeling during developmental transition.