The management of effluent generated by industrial marine aquaculture constitutes a significant challenge for the sustainable development of the sector. In this study, we employed juvenile Urechis unicinctus as a model organism to assess their efficacy in treating effluent derived from industrial Paralichthys olivaceus aquaculture, with an additional focus on elucidating the underlying physiological adaptation mechanisms and intestinal microbial interactions. Four stocking densities (450, 900, 1 350, and 1 800 ind·m⁻²) were implemented for both short-term (168 h) and long-term (30 d) dynamic monitoring. The findings indicated that juvenile U. unicinctus effectively reduced concentrations of suspended solids (SS), chemical oxygen demand (COD), total nitrogen (TN), total phosphorus (TP), ammonia nitrogen ( ${\mathrm{N}\mathrm{H}}_4^{+}\text{-}\mathrm{N}$), nitrite ( ${\mathrm{N}\mathrm{O}}_2^{-}\text{-}\mathrm{N}$), and phosphate ( ${\mathrm{P}\mathrm{O}}_4^{3-}\text{-}\mathrm{P}$) in the effluent. Among the tested densities, the group stocked at 900 ind·m⁻² demonstrated superior treatment performance, achieving removal rates of 35.63% for SS and 26.70% for TP, with an optimal hydraulic retention time identified as 24 h. In a 30-day long-term experiment, under conditions of 900 ind·m⁻², the survival rate of the larvae reached 96.23%, the body mass gain rate reached 20.94%, and the system maintained a stable removal efficiency for the aforementioned water quality parameters. Mechanistic investigations revealed that activities of intestinal digestive enzymes (Lipase, α-amylase, and trypsin) increased markedly during the initial treatment phase before stabilizing. Metagenomic sequencing analysis showed that the intestinal microbiota was predominantly composed of Proteobacteria (65.16%) and Vibrio (46.27%), with species diversity peaking on Day 15. Functional predictions suggested a significant upregulation of genes associated with energy and amino acid metabolism, alongside a downregulation of those involved in carbohydrate and lipid metabolism, indicating an adaptive metabolic shift within the microbial community. Collectively, this study systematically elucidates the synergistic adaptation mechanisms of juvenile U. unicinctus to aquaculture effluent through the regulation of digestive enzymes and functional remodeling of the intestinal microbiome. Furthermore, it confirms that these juveniles can achieve satisfactory growth while effectively purifying effluent, thereby presenting a novel candidate species and providing a theoretical basis for the biological treatment of marine aquaculture wastewater.