Starvation stress is one of the most common environmental challenges faced by aquatic animals, often leading to compensatory growth, a widespread phenomenon in the animal kingdom, especially among aquatic species. The sea cucumber (Apostichopus japonicus), a key marine economic species in China, has been shown to utilize long non-coding RNAs (lncRNAs) in responding to environmental changes, pathogen infections, and tissue regeneration. In this study, strand-specific high-throughput sequencing was employed to analyze transcriptomic data from degenerated intestines of A. japonicus under starvation conditions. High-quality lncRNAs were identified and classified, and key differentially expressed mRNAs and lncRNAs associated with intestinal degradation were screened. A gene interaction network model based on the competing endogenous RNA (ceRNA) theory was then constructed. The analysis revealed that the "AjSOX9/Aja-miR-2012-5p/MSTRG.2956.1 and MSTRG.5699.1" axes, as well as the "AjWNT9B/Aja-miR-200-3p/MSTRG.19757.1 and MSTRG.21788.1" axes, play significant roles in degraded intestines and may promote intestinal regeneration during compensatory growth. Additionally, the "AjFABP2/Aja-miR-9-5p/MSTRG.9667.1" axis appears to regulate energy metabolism under starvation stress. These findings provide valuable insights into the non-coding gene regulatory networks in invertebrates under starvation stress and offer a scientific foundation for developing stress-resistant sea cucumber strains, contributing to the sustainable development of the sea cucumber aquaculture industry.