From 1956 through 1980, Shalev served in the Israel Defense Forces, eventually retiring as a Brigadier General. He commenced his military service in the infantry, first as a foot soldier and then as an officer in the Six-Day War and other events. In 1972–1974, including the Yom Kippur War, Shalev served as Head of the Bureau of the then Chief of Staff, Major General David Elazar. Shalev was part of the international military and political negotiations that followed the war, including the famous Kilometer 101 accords with Egyptian General Gamassi, which eventually led to the Israel–Egypt peace treaty. Following the conclusion of the war, Shalev served in the IDF's Education Corps, becoming Israel's Chief Education Officer. This position included command of IDF Radio, and the task of restoring public confidence in the IDF's abilities. He increased the study of the IDF's battle heritage and combat values, and promoted the leadership training of commanders. Shalev established the Education Corps' central officers' training base and advanced the development of core theory and practice for cultivating Israeli military leadership.
Director of the Culture Authority
Following his retirement from military service, Shalev assumed the position of Director of the Culture Authority in the Ministry of Education and Culture, as well as Chairman of the National Council of Culture and Art. He also served on the boards of a wide range of Israeli museums and cultural institutions. Within these capacities, Shalev was responsible for the formulation and implementation of national policy regarding culture and the arts, and for advancing Israel's ties in these areas with other nations around the world. Among other policies, Shalev earmarked public funding of cultural activities for schoolchildren. He also transformed the Antiquities Department into a national Antiquities Authority. Shalev helped found the Sam Spiegel Film and Television School in Jerusalem. Shalev set up an inter-departmental unit devoted to the absorption of immigrant artists. Its operation facilitated the founding of multiple cultural entities, such as the Ra'anana Orchestra and the Gesher Theater.
Yad Vashem
In 1993 Avner Shalev was appointed Chairman of the Directorate of Yad Vashem. Yad Vashem received the Israel Prize and Princess of Asturias Awards during his tenure. He also received the French Legion of Honor by President Sarkozy, at the Élysée Palace in Paris. Under Shalev's leadership, Yad Vashem has transformed into a leading Israeli and international authority on Holocaust remembrance, documentation, research and education. He established the International School for Holocaust Studies and the International Institute for Holocaust Research. Additionally, Shalev sought to provide better access to fact-based information about the Holocaust by developing and enriching Yad Vashem online presence, available in multiple languages. As leader of Yad Vashem, Shalev has dealt with the controversy over Pope Pius XII, and with the Museum's complicated relations with the Roman Catholic Church. He has sought better access to Vatican archives for the period of Monsignor Pacelli's papacy. In June 2020, Avner Shalev announced his intention to retire by the end of the year.