Harris did both classroom and private teaching, occasionally negotiating special conditions that enabled him to devote the requisite time to composition {e.g., for at least one year during his tenure at The Colorado College, he obtained an arrangement that required him to teach only during the summer, freeing the regular portion of the school term free for the creative work he undertook in his capacity of Composer-in-Residence). The courses he taught over the years ranged from basic theory, counterpoint, and composition (Peabody) to specialized lectures on the development of melodic idiom, analysis of modern music, and J. S. Bach's The Art of the Fugue (Juilliard and Westminster). However, Harris's handling of even the more traditional courses revealed an idiosyncratic approach dominated by his concepts of modality and polychordal, overtone-conditioned harmony. As a result, class discussions often centered around his own music, frequently work-in-progress. As time went on, he found it difficult to adapt to the wide range of idioms his students pursued, and his most congenial, and long-lasting, relationships were generally formed with those who followed his own aesthetics and style.
Among his students were William Schuman, Peter Schickele, John Vincent, Reuel Lahmer, George Lynn (who became director of the Westminster Choir during the 1960s), Robert French (who founded the Louisville Academy of Music), James Niblock, Wray Lundquist (who served as one of his most important copyists), and composer/conductor Keith Clark. Some (e.g., Schuman, Lynn, and French) maintained warm feelings toward and a continuing esteem for Harris in the decades following their studies with him, while others grew apart from their former teacher, occasionally, as with John Vincent, even coming to regard him as a dangerous rival.
Since the 1930s, many of both the composer's and Johana's pupils lived with them, doing music copying, secretarial work, and household chores in exchange for lessons. This was a manifestation of a persistent dream that Harris, in the end, failed to turn into reality: the establishment of a composers' school, an idea hinted at in the aforementioned "self-study plan," and evidently conceived of initially along the lines of the MacDowell Colony and out of the ambiance surrounding Boulanger. He managed a step toward accomplishing it with the establishment in 1960 of the International Institute of Music at the Universidad Interamericana de Puerto Rico (which he unsuccessfully attempted to transfer to the University of the Pacific after leaving Puerto Rico), but aside from this short-lived effort, it appears that the ever-changing "gay guild" of students who shared his home and family routines over several decades are the closest he ever came to this goal.