Background <p>Monocots possess a fibrous root system comprising an embryonic root, crown roots, and lateral roots. The distinct cellular origins highlight the diversity of the initiation mechanism. To date, the distinct initiation mechanisms have been poorly studied. In this study, we conduct a comprehensive transcriptome and DNA methylome assay of these root types during their initiation.</p> Results <p>Our findings indicate significant divergence in transcriptome regulation trajectories with apparent transcriptional activation in post-embryonic root initials (crown root and lateral root) contrasted by suppression in embryonic root generation. Additionally, CHH methylation is dynamically and differentially regulated across the initiation stages of the various root types, and is significantly associated with the short transposon element within the promoter regions of functional genes, which plays crucial roles in determining the genes’ spatiotemporal transcription. Moreover, our work reveals that the activation of <i>DNA glycosylase 702 (DNG702)</i> and repression of <i>Domains Rearranged Methyltransferase 2 (DRM2)</i> play important roles in the erasure of CHH methylation and activation of functional genes during the processes, such as a novel identified key regulatory <i>bZip65</i>, thus directly impacting the initiation of post-embryonic roots in rice.</p> Conclusions <p>Our extensive analysis delineates the landscapes of spatiotemporal transcriptomes and DNA methylomes during the initiation of the three root types in rice, shedding light on the pivotal role of CHH methylation in the spatiotemporal regulation of various key genes, ensuring the successful initiation of distinct root types in rice.</p>