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Abstract In vitro incubations using natural marine communities can provide insight into community structure and function in ways that are challenging through field observations alone. We have designed a minimal metal incubation system for controlled and repeatable experimentation of microbial communities. The systems, dubbed Pelagic Ecosystem Research Incubators (PERIcosms), are 115 L, conical tanks designed to sample suspended, settled, and wall associated material for month long periods. PERIcosms combine some of the ecological advantages of large volume mesocosm incubations with the experimental ease and replication of bottle incubations, and their design is accessible for use by researchers without specialized training or travel to a designated incubation facility. Here, we provide a detailed description for the construction and implementation of PERIcosms and demonstrate their potential to promote replicable, diverse communities for several weeks under clean conditions using time‐series results from two field experiments. One field experiment utilized coastal waters collected from Santa Catalina Island, CA and the other oligotrophic waters collected offshore of Honolulu, HI. Biomass metrics (chlorophyll a and particulate carbon) along with 16S/18S DNA based community composition assessments were conducted to show that communities contained within PERIcosms remained alive and diverse for several weeks using a semi‐continuous culturing approach. We detail trace metal clean techniques that can be used to minimize external contamination, particularly for low dissolved iron environments. PERIcosms have the potential to facilitate natural community incubations which are needed to continue advancing our understanding of microbial ecology and geochemistry.