DNA methylation (5mC) is a gene-regulatory mark mostly associated with transcriptional repression. Research carried out over the last decade has, however, revealed that the amount of 5mC in gene regulatory regions does not always correlate with transcriptional repression. Indeed, a wealth of recent studies have conclusively demonstrated that the interactions between 5mC and transcription factors are highly complex and are far from being understood. Indeed, many transcription factors are not repelled but rather attracted by 5mC, which could potentially serve as an additional mechanism for achieving target-site specificity. Here we set out to explore the 5mC-binding properties of the multifaceted transcriptional regulators FOXK1/2. We reveal that FOXK proteins bind methylated DNA in both anamniotes and mammals and that the FOXK forkhead domain governs this binding. Furthermore, through loss of function assays in zebrafish we demonstrate the embryonic requirements for FOXK1/2 proteins during embryogenesis. RNA-seq profiling of FOXK morphants revealed robust transcriptional misregulation linked to genes associated with cell cycle control, as previously shown in mammals. Overall, our study describes a novel family of 5mC readers and further elaborates on their functions during development and differentiation.