This article describes how inquiry teaching can be directed towards specific content learning goals while allowing for student exploration and validation of hypotheses. Drawing from the Theory of Didactical Situations, the concepts of ‘milieu’ and ‘validation’ are illustrated through two sample biology lessons designed to engage and challenge students in scientific inquiry. The article proposes that these concepts may help teachers design rich learning environments wherein students may pose and test their hypotheses against scientific data. This may in turn help overcome several challenges relating to open-inquiry teaching. Such challenges include divergent student learning outcome or time issues and practical constraints of facilitating inquiry in large classes. The presented approach can help teachers design directed inquiry teaching sequences that can lead to more frequent use of inquiry in teaching thanks to the efficacy of such designs.