The economic value of cotton is based on long, thin, strong, and twisted trichoblast cells that emerge from the ovule epidermis. The mature dried cell reflects the final outcome of a complicated morphogenesis process that includes rapid tapering of the nascent trichoblast, weeks of polarized diffuse growth, followed by a transition to persistent secondary cell wall synthesis. Cellulose microfibril-based anistropic growth control is central to this process. It is widely assumed that the transition to secondary wall synthesis causes a reduced growth rate. However, the biomechanical details that directly link cell wall properties, with fiber morphogenesis is very poorly understood. In this paper, we developed novel imaging quantitative phenotyping, and computational modeling pipelines to analyze fiber growth at a daily resolution. We uncovered unexpected variability in growth rate, cell wall properties, and cell geometry across a broad developmental window. Finite element computational modeling of fiber growth was used to predict how spatial gradients of fiber and matrix material properties can interact to dictate the patterns of shape change. Cellulose patterning is central to the developmental process, and as an initial step toward gaining insight into the molecular control the expression profiles of a broad set of genes known to orchestrate cellulose biosynthesis were quantified across the same developmental timeline and correlated with fiber phenotypes. This analysis identified specific Gossypium hirsutum targets for fiber quality improvement.