Despite the hope of this new charter, the building of Dillard University was tempered by its context of Jim Crow America. Many local Whites took concern with the possibility of a Black president presiding over White faculty members. Similarly, the increased numbers of African American bus riders in the Gentilly area disturbed some White sensibilities. As an influential and diplomatic member of Dillard's board of trustees, Edgar B. Stern Sr suggested Will W. Alexander as a suitable compromise. Will W. Alexander, a white Southern preacher, was Dillard's first acting president (1935–1936), whose experience as the director of the Commission on Interracial Cooperation proved valuable. Dillard University opened its doors in the fall of 1935, and was able to attract a number of prominent scholars, such as Horace Mann Bond, psychology and education; Frederick Douglass Hall, music; Lawrence D. Reddick, history; and St. Clair Drake, sociology and anthropology.
In August 2005, the campus, not far from the lower levee breach of the London Avenue Canal, suffered extensive flood damage in the aftermath of Hurricane Katrina. Nelson Hall was destroyed by a fire. A bus fire also destroyed belongings of 37 students who were in the process of being evacuated. In spring 2006, the students of Dillard University took their normal classes at The New Orleans World Trade Center and The New Orleans Hilton Riverside Hotel. As is tradition, Dillard held graduation on the Rosa Freeman Keller Avenue of the Oaks in July 2006. Students returned to campus in September 2006.
In 2003, musician Ray Charles added a provision in his will to endow a $1 million professorship of African-American culinary history at Dillard. It is the first such position in the country.
The campus has the following buildings on its grounds:
DUICEF (Dillard University International Center for Economic Freedom) was dedicated in 2004. It houses the offices of the Division of Education & Psychology and the Division of Social Sciences, and computer and language laboratories.
Howard House, built in 1936, was originally a guest house, but currently is home to the business program. The building was named in honor of New Orleans native Alvin Pike Howard (1889–1937), successful businessman, former professor of Tulane University and former director of Hibernia National Bank; he is a noteworthy contributor to the development of Dillard University.
The Professional Schools Building is the newest academic building on campus. It was dedicated in 2010. The building is home to academic and research programs for the College of Business, School of Nursing, School of Public Health, and the Department of Science, Technology, Engineering and Mathematics.
Rosenwald Hall is a hall at Dillard University. Dillard's first permanent building was originally the campus library. It was built in May 1934. The building is named in honor of philanthropist Julius Rosenwald, to whom the building was dedicated in June 1948. This building houses the university's administrative offices and was under construction due to damage in the aftermath of Hurricane Katrina. It was back in operation in the fall of 2008.
Samuel DuBois Cook Fine Arts and Communications Center at Dillard University, New Orleans, was built in 1993. The building is named in honor of Dillard University's sixth president, Dr. Samuel DuBois Cook. With his tenure came the start of the modernization of Dillard University's infrastructure. In the building are the Fine Arts Gallery and studios, state-of-the-art television and recording studios, the Music Department, the Drama Department and a theater, and a radio station.
Stern Hall is a hall at Dillard University. Dillard's science building was built in 1952. It is named in honor of Edgar Bloom Stern, a prominent financier and philanthropist of New Orleans. The building was renovated in 1952 and again in 1968. In the building are the Division of Nursing, Division of Natural Sciences, two computer labs, Biology, Chemistry and Physics labs as well as a learning center sponsored by the Louisiana Alliance for Minority Participation (LAMP) program.
Will W. Alexander Library is Dillard University's library. It was built in 1961. The library was dedicated in honor of the first acting president of Dillard University, the Rev. Will W. Alexander on October 22, 1961. The library houses an extensive collection of books, journals, microform and newspapers, as well as such historical documents as the papers of the American Missionary Association of the United Church of Christ. The library was damaged in the aftermath of Hurricane Katrina and reopened as a state-of-the-art facility in April 2008.
Lawless Memorial Chapel is Dillard University's chapel. It was built in 1955. Chapel was dedicated to the memory of Dr. Alfred Lawless Jr. and his son Theodore K. Lawless M.D. on October 23, 1955. Now named Lawless Assembly Hall, it is the only building on Dillard's campus that did not suffer flood damage in the aftermath of Hurricane Katrina.
Camphor Hall is a hall at Dillard University, New Orleans. It was built in 1947. This female dormitory was originally a male dormitory. The building was named in honor of a Louisiana native, educator and missionary, Bishop Alexander Priestly Camphor.
Hartzell Hall is a dormitory at Dillard University. It was built in 1935. Hartzell is named in honor of Joseph Crane Hartzell, a missionary bishop for the Methodist Episcopal Church. The building was originally a junior and senior female dormitory, and re-opened in the fall of 2013.
Nelson Complex consisted of three modular buildings that served as undergraduate housing for students. Named after William Nelson, the first African American president of the university, it was destroyed by fire during Hurricane Katrina.
Straight Hall is a dormitory at Dillard University. It was built in 1936 and renovated in 1957, Straight Hall was originally a female dormitory in its earliest days. The building is named in honor of Seymour Straight, president of the Board of Trustees of Straight College, which opened in 1869 and later in 1930 merged with New Orleans University to form Dillard University. Re-opened in the spring of 2013.
Williams Hall is a female dormitory building located to the left of Kearny hall. It was dedicated in honor of noted New Orleanian educator and philanthropist Fannie C. Williams (1882–1980) in June 1946. The building was renovated in 2000 and became a co-ed dormitory in 2014.
Dent Hall at Dillard University, New Orleans, is the university's gymnasium. It was named in honor of Dr. Albert W. Dent, the university's third president. It was built in 1969 at the end of his service. Dent Hall is the home of the Bleu Devils and the Lady Bleu Devils basketball teams (Athletics Department). In this building are The Division of Campus Life, Career Services, Student Development, Student Government Association, the Daniel C. Thompson/Samuel Dubois Cook Honors Program, offices, classrooms, computer labs, a dance studio, a weight center and a newly renovated swimming pool.
Henson Hall is Dillard University's old gymnasium, which was built in 1950 and renovated in 1990. The building is named in honor of an explorer and co-discoverer of the North Pole, Matthew Alexander Henson. He was the first human of African descent to reach the North Pole. The university's bookstore and temporary library are housed in Henson Hall due to space constraints following Hurricane Katrina.
Kearny Hall is the student center at Dillard University. It was built in 1935 and renovated in 1966 and 1996. This building is named in honor of New Orleanian Warren Kearny, Trustee of Dillard University. Kearny Hall is located at the center of the campus. In the building are a lounge area, post office, cafeteria, food service offices, as well as the Student Government Association office.
Built in 1936, the president's residence has been renovated three times: 1964, 1972 and 1997. It has been home to six of the seven presidents of Dillard University. It now serves as the Alumni House.