Miller is an exponent of the existence of the so-called "unwritten teachings" of Plato: the controversial idea that Plato taught advanced concepts to his students at the Academy beyond those explicitly discussed by Socrates in Plato's dialogues. The idea, which is dismissed by many Plato scholars, is based on a brief description of such teachings by Aristotle in his Metaphysics. The Seventh Letter, which was attributed to Plato in antiquity, was later considered inauthentic for a time, and is now regarded by most scholars as genuine, also includes indications of such teachings. Miller has argued that evidence of these teachings can be found in the dialogues, but only through careful reading of structure and irony within them.
Miller's work has focused on several of the late dialogues, notably the Parmenides, Statesman, and Philebus, as well as the Republic. In his book on the Parmenides, Miller argues that the eight bewildering and contradictory hypotheses that end the dialogue form an ironic guide that allows the informed reader to interpret the whole, revealing through what Miller has called "psychagogy"—a transformation of the philosophical disciple's soul—the true nature of Plato's conception of the forms. That is, the ultimate purpose of the text is not to teach the reader didactically but to draw them into a different kind of thinking.
- The Philosopher in Plato's Statesman. The Hague: Martinus Nijhoff, 1980. Reprinted with additional material, Las Vegas: Parmenides, 2004, ISBN 978-1-930972-16-2
- Plato's Parmenides: The Conversion of the Soul. Princeton: Princeton UP, 1986. Reprinted University Park: Pennsylvania State UP, 1991.