Changes in DNA methylation in specific coding or non-coding regions can influence development and potentially divergence in traits within species and groups. While the impact of epigenetic variation on developmental pathways associated with evolutionary divergence is the focus of intense investigation, few studies have looked at recently diverged systems. Phenotypic diversity between closely related populations of Arctic charr (Salvelinus alpinus), which diverged within the last 10 000 years, offers an interesting ecological model to address such effects. Using bisulfite sequencing, we studied general DNA methylation patterns during development in the four sympatric morphs of Arctic charr from Lake Thingvallavatn. The data revealed strong differences between developmental timepoints and between morphs (mainly along the benthic – limnetic axis), both at single CpG sites and in 1,000bp-regions. Genes located close to differentially methylated CpG sites were involved in nucleosome assembly, regulation of osteoclast differentiation, and cell-matrix adhesion. Differentially methylated regions were enriched in tRNA and rRNA sequences, and half of them were located close to transcription start sites. The expression of 14 genes showing methylation differences over time or between morphs was further investigated by qPCR and nine of these were found to be differentially expressed between morphs. Four genes (ARHGEF37-like, H3-like, MPP3 and MEGF9) showed a correlation between methylation and expression. Lastly, histone gene clusters displayed interesting methylation differences between timepoints and morphs, as well as intragenic methylation variation. The results presented here provide a motivation for further studies on the contribution of epigenetic traits, such as DNA methylation, to phenotypic diversity and developmental mechanisms.