In 1982, Indyk began working as a research director for the American Israel Public Affairs Committee (AIPAC), a pro-Israel lobbying group in Washington. After that, Indyk served eight years as the founding Executive Director of the Washington Institute for Near East Policy, a research institute specializing in Arab-Israel relations. He has also been an adjunct professor at the Johns Hopkins School of Advanced International Studies where he taught Israeli politics and foreign policy.
He has taught at the Middle East Institute at Columbia University, the Moshe Dayan Center for Middle Eastern and African Studies at Tel Aviv University, and the Department of Politics at Macquarie University in Sydney, Australia. Indyk has published widely on U.S. policy toward the Arab-Israeli peace process, on U.S.-Israeli relations, and on the threats of Middle East stability posed by Iraq and Iran.
He served as special assistant to U.S. President Bill Clinton and as senior director of Near East and South Asian Affairs at the United States National Security Council. While at the NSC, he served as principal adviser to the President and the National Security Advisor on Arab-Israeli issues, Iraq, Iran, and South Asia. He was a senior member of Secretary of State Warren Christopher's Middle East peace team and served as the White House representative on the U.S. Israel Science and Technology Commission.
He served two stints as United States Ambassador to Israel, from April 1995 to September 1997 and from January 2000 to July 2001 and was the first and so far, the only, foreign-born US Ambassador to Israel.
Currently, Indyk directs the Saban Center for Middle East Policy. He currently focuses on the Clinton administration’s diplomacy and the Arab-Israeli conflict.