DNA methylation, also known as 5-methylcytosine, is an epigenetic modification that has crucial functions in multiple important biological processes in fish, such as gonadal development. The cellular DNA methylation level is tightly regulated by DNA methyltransferases (Dnmt). However, detailed investigations of this family in fish are very scarce. In this study, our results confirmed that teleost genomes contain 4 to 16 Dnmt genes, with diversity likely resulting from a combination of whole-genome duplication (WGD), tandem duplication, and gene loss. Differences were observed in tissue distribution, transcription abundance, and protein structure of Dnmt duplicates, supporting their subfunctionalization or neofunctionalization after duplication. Interestingly, we found that fish Dnmt3b duplicates likely have acquired the functions of mammalian Dnmt3l, which may compensate for the absence of fish Dnmt3l. Furthermore, transcriptome analysis and qPCR results indicated that DNA methyltransferase genes (Dnmt1, Dnmt3aa, Dnmt3ab, Dnmt3ba, and Dnmt3bb.1) possibly play important roles in the natural sex change of protandrous hermaphrodite blackhead seabream (Acanthopagrus schlegelii) and inferred that global remodeling of gonadal DNA methylation, regulated by DNA methyltransferase genes, was closely associated with sex change in sequentially hermaphroditic fishes. Overall, our results may help provide a better understanding of the evolution and function of DNA methyltransferases in fish.