In this paper, drawing on evidence internal to the Platonic dialogues (supplemented with some ancient testimonia), I answer the question, “How did Plato teach in the Academy?” My reconstruction of Plato’s pedagogy in the Academy is that there was a single person who read the dialogue aloud like a rhapsode (this is in contrast to the dramatic theatrical hypothesis, in which several speakers function as actors in the performance of a dialogue). After the rhapsodic reading, students were allowed to ask that portions of the text to be re-read, to ask a question about the text, and were encouraged to enter into a broader conversation about the topic and themes brought out by the text. This later pedagogical method of interrogating and investigating a dialogue is of more importance than the mere reading of a dialogue. I contend that Plato’s experiences teaching were woven into some of the dialogues, and that Plato’s pedagogy reflects some of the ways that he taught in the Academy. I propose that excellent points made by students may have been written into revised forms of the dialogue. And not only good points, but also mistakes in reasoning may have been added into the dialogues. I suggest that the way certain dialogues are organized with “guest lecturers” and “tag-team” philosophical debates reflect Plato’s pedagogy in the Academy. Plato’s broadmindedness, his openness to various and opposing viewpoints, is also evident from both outside and inside of the dialogue. Lastly, drawing on the idea of Socratic mimēsis, I give a plausible curriculum for how Plato may have used the dialogues to teach them: he had his students “play” with them. Plato may have asked his students to enter into the roles of the characters in the dialogues to better understand them and the type of person they represent. Plato may have also asked students to take over from the position of the character in the dialogue and to suggest a better, truer account of things than what the characters said or did.