The water flea Daphnia carinata is emerging as a new model for biological studies due to its natural cyclical parthenogenesis and small genome. However, no genomic information for the D. carinata is currently available. Here, we reported a chromosome-scale genome assembly of D. carinata. The assembled D. carinata (WSL) genome was consisted of 131.58 Mb, and 92.23% (121.36 Mb) of the assembly was anchored onto 10 chromosomes. Basing on the whole genome information, we further compared the transcriptomic and epigenomic characterization among parthenogenetic females (PF), sexual females (SF) and males (M) in D. carinata. Transcriptomic analysis showed that the highly expressed genes in M were mainly grouped into the cuticle, phototransduction, hypoxia-response, sex differentiation, and methyl farnesoate synthesis. Besides, compared to M and SF, the highly expressed genes in PF were mainly grouped into energy metabolism, mitosis, DNA replication, and RNA splicing. miRNAomic analysis showed that several miRNA-mRNA pairs may be the functional modules in the reproductive regulation of D. carinata, such as novel-miR-4—brat, novel-miR-21—lin-9 pairs, novel-miR-110—gl, novel-miR-4—eIF3-S9. The whole-genome DNA methylation analysis showed that genome-wide methylation rate was very low in D. carinata, and DNA methylation sites were mainly enriched in the gene body region. Comparative analysis showed that the genome-wide methylation rate in PF was higher than that in SF and M. Differentially methylation region-related genes were all mainly grouped in metabolic process, catalytic activity, binding/ion binding, and cellular process.