Aberrant DNA methylation plays a critical role in the development and progression of colorectal cancer (CRC), which has high incidence and mortality rates in Korea. A variety of CRC-associated methylation markers for cancer diagnosis and prognosis have been developed; however, those markers have not been validated for Korean patients because of the lack of comprehensive clinical and methylome data. Here, we obtained reliable methylation profiles of 228 tumor, 103 adjacent normal, and two unmatched normal colon tissues from Korean patients with CRC using an Illumina Infinium EPIC array, and the data were corrected for biological and experiment biases. A comparative methylome analysis confirmed the previous findings that hypermethylated positions in the tumor were highly enriched in CpG island and promoter, 5' untranslated, and first exon regions, whereas hypomethylated positions were enriched in open-sea regions that are considerably distant from CpG islands. After applying a CpG island methylator phenotype to the methylome data of tumor samples to stratify the CRC patients, we consolidated the previously established clinicopathological findings that the tumors with high CIMP signatures were significantly enriched in the right colon and showed a higher prevalence of microsatellite instability status and MLH1 methylation than the tumors with low or non-CIMP signatures. Therefore, our methylome analysis and dataset can provide insights into the application of the CRC-associated methylation markers for Korean patients, regarding cancer diagnosis and prognosis.