The colonial system of integration (CSI) provides intracolonial nutrient supply in many gymnolaemate bryozoans. In Ctenostomata, its presence is known for species with stolonal colonies, for example, vesicularioideans, but its structure is almost unexplored. The CSI is thought to be absent in alcyonidioideans and other ctenostomes. Here, we present the first detailed description of the CSI ultrastructure in both autozooids and kenozooids of two vesicularioideans, Buskia nitens and Amathia gracilis, and two alcyonidioideans, Alcyonidium hirsutum and Flustrellidra hispida. We revealed differences in the endocyst structure: in studied alcyonioidioideans, it comprises the epidermis, extracellular matrix and coelomic lining, while in the studied vesicularioideans, it includes only the epidermis. In vesicularioidean autozooids, the main CSI cord and the most distal part of the muscular funiculus originate together as a single structure near the caecum apex. However, at a short distance basally, they separate and run to different sites: the main CSI cord reaches the communication pore, and the muscular funiculus attaches to the cystid wall in the proximal part of the autozooids. The CSI in alcyonidioidean autozooids includes a central part, comprising several strands running from the caecum and pylorus to the cystid walls, and a peripheral part, which is located between the epidermis and peritoneum of the cystid walls and reaches the communication pores. The autozooidal CSI in the studied alcyonidioids never reaches kenozooidal communication pores. Nevertheless, the CSI is present in kenozooids of F. hispida; its structure corresponds to that of the peripheral part of the CSI in autozooids. These findings suggest that the CSI likely originated rather early in bryozoan evolution, and its putative initial function is nutrient transport to budding sites and zooids undergoing degeneration‐regeneration cycle.