For the past ten years, the developmental model of microbial biofilm formation has served as the major conceptual framework for biofilm research; however, the paradigmatic value of this model has begun to be challenged by the research community. Here, we critically evaluate recent data to determine whether biofilm formation satisfies the criteria requisite of a developmental system. We contend that the developmental model of biofilm formation must be approached as a model in need of further validation, rather than utilized as a platform on which to base empirical research and scientific inference. With this in mind, we explore the experimental approaches required to further our understanding of the biofilm phenotype, highlighting evolutionary and ecological approaches as a natural complement to rigorous mechanistic studies into the causal basis of biofilm formation. Finally, we discuss a second model of biofilm formation that serves as a counterpoint to our discussion of the developmental model. Our hope is that this article will provide a platform for discussion about the conceptual underpinnings of biofilm formation and the impact of such frameworks on shaping the questions we ask, and the answers we uncover, during our research into these microbial communities.