The domestic chicken (Gallus gallus domesticus) is the globally most important source of commercially produced meat. While genetic approaches have played an important role in the development of chicken stocks, little is known about chicken epigenetics. We have systematically analyzed the chicken DNA methylation machinery and DNA methylation landscape. While overall DNA methylation distribution was similar to mammals, sperm DNA appeared hypomethylated, which correlates with the absence of the DNMT3L cofactor in the chicken genome. Additional analysis revealed the presence of low-methylated regions, which are conserved gene regulatory elements that show tissue-specific methylation patterns. We also used whole-genome bisulfite sequencing to generate 56 single-base resolution methylomes from various tissues and developmental time points to establish an LMR-based DNA methylation clock for broiler chicken age prediction. This clock was used to demonstrate epigenetic age acceleration in animals with experimentally induced inflammation. Our study provides detailed insights into the chicken methylome and suggests a novel application of the DNA methylation clock as a marker for livestock health.