Joëlle Proust was recruited in 1976 as a researcher at French Centre National de la Recherche Scientifique (CNRS) in the domain of the history and philosophy of logic. Her comparative history of logical truth won her the CNRS bronze medal (Questions of Form, Minnesota Press, 1989).

From 1990 on, Proust expanded her area of philosophical interest from logic to mind. She addressed the question of how to naturalize representational capacity. She then studied action awareness, its impairments in schizophrenia, and the structure of mental agency, a question often viewed with suspicion in cognitive science and in the naturalistic philosophy of mind. Using a control view of action, she analyses metacognition as a crucial functional ingredient in mental action (e.g. controlled remembering, perceiving, reasoning), whose functional equivalent for bodily action is motor control through anticipatory sensory feedback.

She assembled an interdisciplinary, 7-team ESF- EUROCORE project (2006-9), aimed at exploring the phylogeny and ontogeny of metacognition, and its relations with consciousness. In 2010, Proust was awarded an advanced grant by the European Research Council in order to study the sensitivity of Western and Eastern children and adults to different epistemic norms such as intelligibility, truth, coherence, relevance and consensus, as displayed in their metacognitive evaluations. This international project, called DIVIDNORM, involved a collaboration between 3 European academic Institutions, a Japanese developmental lab and a Mexican Anthropological Research team. It was completed in December 2016. It generated many publications  in Philosophy, Developmental and adult Psychology, Neuroscience  and Anthropology. A collective book about Metacognitive Diversity, to appear in 2018, addresses examines normative sensitivity across culture from  anthropological, developmental,  linguistic and philosophical perspectives.

Proust was a co-founder of several scientific societies, such as SOPHA (the Society for Analytic Philosophy in the French language), HOPOS (The International Society for the History of Philosophy of Science), ESAP (the European Society for Analytic Philosophy), and ESPP (the European Society for Philosophy and Psychology). She presently works at Institut Jean-Nicod, Ecole Normale Supérieure in Paris. Since January 2018, she has joined the newly created Scientific Council of National Education chaired by Stanislas Dehaene. Together with Sid Kouider, she has been asked to propose innovative pedagogical practices based on metacognitive studies, meant to enhance self-confidence in pupils and fight school unequality.