The dramatic expansion of online learning in U.S. higher education has been accompanied by a notable shift in the demographics of students enrolled in these courses. International students are among those participating in online courses in growing numbers, infusing the virtual space with greater cultural diversity. Many instructors are unprepared for this change. Culture plays an influential role in how we learn, yet instructors rarely consider it in the design and facilitation of their online courses. This can have a negative impact on learners and often affects international students in disproportionate ways. The purpose of this study was to identify essential competencies that higher education instructors at U.S. institutions need in order to create online courses that are culturally inclusive and support the success of international students. Using a Delphi approach, I solicited input from 29 scholars and practitioners from across the U.S. who were experts in international education, international student support services, intercultural competence, culturally responsive pedagogy, and instructional design for online learning. Through three iterative rounds of questionnaires, I drew on panelists’ expertise in order to determine what competencies instructors need in order to design and facilitate inclusive online courses; to vet and rate an extensive list of knowledge, attitudes and skills in terms of their usefulness in promoting inclusion; and to distill these into a list of 14 most essential competencies. The competencies that emerged from this study can equip instructors to better serve international students through the design and facilitation of online courses that are culturally inclusive. The findings can also be useful to centers for teaching and learning and campus administrators, who can refer to the competencies in developing systems, policies, resources, and training opportunities to better support instructors and international students at their institutions.