<p>Understanding genetic and biological diversity within a co-managed species complex can play an essential role in effective management strategies. This is particularly important in commercially and ecologically important stocks, such as the Vermilion/Sunset Rockfish complex. Vermilion (<i>Sebastes miniatus</i>) and Sunset (<i>S. crocotulus/S. miniatus Type 1</i>) Rockfish are part of a cryptic species complex with high value to the Southern California recreational fishery. Attempts to assess this complex have been complicated by an inability to easily distinguish these species visually. Here, we assessed the inter- and intraspecific genetic divergence within the Vermilion/Sunset cryptic species complex using genotyping-in-thousands by sequence (GT-seq) and low-coverage whole genome sequencing (lcWGS). We found that while Sunset Rockfish only exhibits subtle structure across its range, Vermilion Rockfish consists of three distinct cryptic lineages. The genetic divergence among these lineages (<i>F</i>_ST = 0.07–0.16) is higher than the divergence between many recognized species pairs, and there is little evidence for contemporary gene flow among them. Additionally, we found significant biological and ecological differentiation with all three groups found at significantly different depths. We found an extremely low rate of hybridization between the two species (0.27% of samples) with most hybrids exhibiting intermediate biological and ecological characteristics. Furthermore, we investigated the potential genomic bases underlying these differences with lcWGS data. Results from this study help clarify the overall diversity and distinctness of groups within this complex, as well as provide specific information for future stock assessments and management strategies.</p>