The contributions that control of cell proliferation and cell growth make to developmental regulation of organ and body size remain poorly explored, particularly with respect to endocycles in polyploid tissues. The epithelium of the marine chordate Oikopleura dioica is composed of a fixed number of cells grouped in territories according to gene-specific expression and nuclear sizes and shapes. As the animal grows 10-fold during the life cycle, epithelial cells increase in size differentially as a function of their spatial position. We show that this cellular pattern reflected differences in ploidy levels ranging from 34 to 1,300 C. The diverse ploidy levels in defined cellular fields resulted both from different timing of entry into endocycles and from cell-specific regulation of endocycle lengths. Throughout the life cycle, differential cell size and ploidy increases were accompanied by field-specific profiles of progressive reductions in G-phase duration. Endocycles were asynchronous among cells of a given epithelial territory, but at the resolution of individual cells, both DNA replication timing and ploidy levels were bilaterally symmetric. The transparent, accessible, oikoplastic epithelium is a model of choice for the study of endoreduplication in the context of pattern formation and growth.