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Simple Summary: This study investigates the impact of DNA methylation on collagen deposition in the skin of Dezhou donkeys, a breed valued for its thick, flexible skin with medicinal properties. Utilizing whole genome bisulfite sequencing (WGBS) and RNA sequencing (RNA-seq), the research analyzes the epigenetic landscape and gene expression profiles across three developmental stages of Dezhou donkeys. The study identifies numerous differentially methylated genes related to collagen deposition, such as COL1A1, COL1A2, and MMPs, highlighting an inverse relationship between gene expression and DNA methylation near transcription start sites. The findings of our study reveal the significant regulatory role of DNA methylation in skin collagen deposition, offering insights for genetic improvement and selective breeding to enhance skin quality in Dezhou donkeys. Our current research adds to the foundational knowledge of collagen deposition mechanisms, contributing to the fields of molecular biology and animal husbandry. DNA methylation represents a predominant epigenetic modification with broad implications in various biological functions. Its role is particularly significant in the process of collagen deposition, a fundamental aspect of dermal development in donkeys. Despite its critical involvement, the mechanistic insights into how DNA methylation influences collagen deposition in donkey skin remain limited. In this study, we employed whole genome bisulfite sequencing (WGBS) and RNA sequencing (RNA-seq) to investigate the epigenetic landscape and gene expression profiles in the dorsal skin tissues of Dezhou donkeys across three developmental stages: embryonic (YD), juvenile (2-year-old, MD), and mature (8-year-old, OD). Our analysis identified numerous differentially methylated genes that play pivotal roles in skin collagen deposition and overall skin maturation, including but not limited to COL1A1, COL1A2, COL3A1, COL4A1, COL4A2, GLUL, SFRP2, FOSL1, SERPINE1, MMP1, MMP2, MMP9, and MMP13. Notably, we observed an inverse relationship between gene expression and DNA methylation proximal to transcription start sites (TSSs), whereas a direct correlation was detected in regions close to transcription termination sites (TTSs). Detailed bisulfite sequencing analyses of the COL1A1 promoter region revealed a low methylation status during the embryonic stage, correlating with elevated transcriptional activity and gene expression levels. Collectively, our findings elucidate key genetic markers associated with collagen deposition in the skin of Dezhou donkeys, underscoring the significant regulatory role of DNA methylation. This research work contributes to the foundational knowledge necessary for the genetic improvement and selective breeding of Dezhou donkeys, aiming to enhance skin quality attributes. [ABSTRACT FROM AUTHOR]