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Summary Polyploidy is an important evolutionary force, yet epigenetic mechanisms, such as DNA methylation, that regulate genome‐wide expression of duplicated genes remain largely unknown. Here, we useTragopogon(Asteraceae) as a model system to discover patterns and temporal dynamics of DNA methylation in recently formed polyploids.The naturally occurring allotetraploidTragopogon miscellusformed in the last 95–100 yr from parental diploidsTragopogon dubiusandT. pratensis. We profiled the DNA methylomes of these three species using whole‐genome bisulfite sequencing.Genome‐wide methylation levels inT. miscelluswere intermediate between its diploid parents. However, nonadditive CG and CHG methylation occurred in transposable elements (TEs), with variation among TE types. Most differentially methylated regions (DMRs) showed parental legacy, but some novel DMRs were detected in the polyploid. Differentially methylated genes (DMGs) were also identified and characterized.This study provides the first assessment of both overall and locus‐specific patterns of DNA methylation in a recent natural allopolyploid and shows that novel methylation variants can be generated rapidly after polyploid formation. Together, these results demonstrate that mechanisms to regulate duplicate gene expression may arise soon after allopolyploid formation and that these mechanisms vary among genes.