Huntington's disease (HD) is a genetic neurodegenerative disorder, caused by CAG repeat expansion (>39) coding for poly-glutamine (polyQ) tract in the Huntingtin (HTT) gene. Although HD is late onset, it was shown to have an early neurodevelopmental component. In addition, DNA methylation was shown in adults to be an important epigenetic mechanism involved in HD. Here we sought to explore early pre-symptomatic neurodevelopmental alterations in DNA methylation using cerebral organoids from juvenile forms of isogenic HD pluripotent cells. We find wide-spread DNA demethylation in the mutant cells (72Q and 180Q), which also displayed a polyQ length-dependent increased predicted epigenetic age. We show that the de-methylated positions are highly enriched in DNMT3B motif and, using structural modeling, co-IP and FRET imaging analyses, we demonstrate polyQ-length-dependent DNMT3B-HTT interactions. To explore the effects of de-methylation on gene expression, we compared RNA-seq from HTT-knockout (KO) and 72Q organoids. While premature neuronal differentiation was shared between the KO and HD systems, supporting a loss-of-function origin, some pathways were uniquely altered in the 72Q-iPSCs organoids, suggesting an additional gain-of-function effect. Focusing on upregulated genes with hypomethylated promoters, revealed similar pathways suggesting a connection to DNA demethylation. Finally, single cell RNA-seq confirmed accelerated neurogenesis in the HD organoids. Taken together, our findings reveal fundamental neurodevelopmental and epigenetic defects in the early stages of neurogenesis in HD models, highlighting DNA methylation as a central pathway in early HD.