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The evolutionary direction of gonochorism and hermaphroditism is an intriguing mystery to be solved. The special transient hermaphroditic stage makes the little yellow croaker (Larimichthys polyactis) an appealing model for studying hermaphrodite formation. However, the origin and evolutionary relationship between ofL. polyactisandLarimichthys crocea, the most famous commercial fish species in East Asia, remain unclear. Here, we report the sequence of theL. polyactisgenome, which we found is ~706 Mb long (contig N50 = 1.21 Mb and scaffold N50 = 4.52 Mb) and contains 25,233 protein‐coding genes. Phylogenomic analysis suggested thatL. polyactisdiverged from the common ancestor,L. crocea, approximately 25.4 million years ago. Our high‐quality genome assembly enabled comparative genomic analysis, which revealed several within‐chromosome rearrangements and translocations, without major chromosome fission or fusion events between the two species. Thedmrt1gene was identified as the male‐specific gene inL. polyactis. Transcriptome analysis showed that the expression ofdmrt1and its upstream regulatory gene (rnf183) were both sexually dimorphic.Rnf183, unlike its two paraloguesrnf223andrnf225, is only present inLarimichthysandLatesbut not in other teleost species, suggesting that it originated from lineage‐specific duplication or was lost in other teleosts.Phylogenetic analysis shows that the hermaphrodite stage in maleL. polyactismay be explained by the sequence evolution ofdmrt1. Decoding theL. polyactisgenome not only provides insight into the genetic underpinnings of hermaphrodite evolution, but also provides valuable information for enhancing fish aquaculture.