show Abstracthide AbstractSong learning in zebra finches is a prototypical example of a complex learned behavior, yet knowledge on the underlying molecular processes is limited. Therefore, we characterized transcriptomic (RNA sequencing) and epigenomic (RRBS, reduced representation bisulfite sequencing; immunofluorescence) dynamics in matched zebra finch telencephalon samples of both sexes from 1 day post hatching (1 dph) to adulthood, spanning the critical period for song learning (20 dph and 65 dph). We identified extensive transcriptional neurodevelopmental changes during postnatal telencephalon development. DNA (hydroxy)methylation was very low, yet increased over time, particularly in song control nuclei. Only a small fraction of the massive differential expression in the developing zebra finch telencephalon could be explained by differential CpG and CpH DNA methylation. However, a strong association between DNA methylation and age dependent gene expression was found for various transcription factors (i.a. OTX2, AR and FOS) involved in neurodevelopment. Additionally, genomic regions featured by age dependent differential methylation in differentially expressed genes were significantly enriched for specific transcription factor binding motifs. Incomplete dosage compensation was found to be largely responsible for sexually dimorphic gene expression, with dosage compensation increasing throughout life. In conclusion, our results indicate that DNA methylation regulates neurodevelopmental gene expression dynamics through steering transcription factor activity, but does not explain sexually dimorphic gene expression patterns in zebra finch telencephalon. Overall design: For each sex per time point (1 day post hatch (dph), 20dph, 65dph and adult), 3 independent biological replicates were sequenced, resulting in a total of 24 samples. To increase power, each of these biological replicates consisted of a pool of RNA of 3 telencephalons in equal proportions.