Regeneration of lost or damaged appendages is a widespread and ecologically important ability in the animal kingdom, and also of great significance to developing regenerative medicine. The operculum of serpulid polychaetes is one among the many diverse appendages found in the lophotrochozoan superphylum, a clade hitherto understudied with respect to the mechanisms of appendage regeneration. In this study, we establish the normal time course of opercular regeneration in the serpulid Pomatoceros lamarckii and describe cell proliferation patterns in the regenerating opercular filament. The P. lamarckii operculum regenerates through a rapid and consistent series of morphogenetic events. Based on 5-bromo-2′-deoxyuridine (BrdU) labeling and anti-phosphohistone H3 immunohistochemistry, opercular regeneration appears to be a mixture of an early morphallactic stage, and a later phase characterized by widespread proliferative activity within the opercular filament. Tracking residual pigmentation suggests that the distal part of the stump gives rise to the most distal structures of the operculum via morphallactic remodeling, whereas more proximal structures are derived from the proximal stump. Our work underscores the diversity of regenerative strategies employed by animals and introduces P. lamarckii as an emerging model of appendage regeneration. J. Exp. Zool. (Mol. Dev. Evol.) 322B: 257–268, 2014. © 2014 Wiley Periodicals, Inc.