This study aimed to identify a potentially harmful species occurring in sea cucumber (Apostichopus japonicus) culture ponds and investigate their genetic relationships in different sea cucumber culture areas. The worms were identified using both morphological and molecular biological methods. The genetic diversity and genetic structure of two geographic populations in Dongying and Qingdao, Shandong, were analyzed based on 18S rDNA, CO I, and ITS gene sequences. The results indicate that the worm is red in appearance, measuring between 7.94–25.27 mm in length, and 0.65–0.94 mm in width. Its head was either conical or obtuse-rounded. The thorax was divided into nine segments, with the first to seventh segments containing bundles of hairy bristles. Mature males possess hook-like reproductive spines on the dorsal side of the body at the eighth and ninth thoracic segments, along with an elliptical reproductive tube between the seventh and eighth thoracic segments. Mature females have paired ovaries on their abdominal sides. The body was rounded on the dorsal side and flatter on the abdominal side, with no gills behind the abdomen. The tail end was anal. Based on the phylogenetic tree and sequence comparison of the mitochondrial CO I gene, it was found to be clustered into a clade with Capitella teleta with 99.11% sequence similarity. Eventually, based on the morphological characteristics and CO I gene analysis, the worms were identified as C. teleta. Genetic evolutionary analyses of the CO I gene sequences of Capitella from different areas revealed that C. teleta from Dongying, in China, was more closely related to C. teleta from Korea and C. teleta from Japan, re-confirming that the red worms in sea cucumber culture ponds were C. teleta. The genetic diversity and AMOVA analysis results of C. teleta populations from Dongying and Qingdao showed that the genetic diversity of the Dongying group was higher than that of the Qingdao group; the two geographic populations of C. teleta were distantly related, and there was a degree of genetic differentiation between the two groups. This study clarified the specific species of Capitella in sea cucumber cultures and the genetic relationships between C. teleta populations in different sea cucumber culture areas. These results provide a scientific basis for the development of healthy aquaculture technologies for sea cucumber culture.