In the 1920s, Kirk was executive officer of the presidential yacht and served as presidential naval aide. He next served as the gunnery officer on the battleship Maryland. Kirk graduated from the Naval War College in 1929 and then was an instructor there for two years. In 1931, he received his first command, a destroyer, and from 1933 to 1936, he was in the Office of the Chief of Naval Operations. He was the executive officer of the battleship West Virginia before taking command of the light cruiser Milwaukee and serving as operations officer to the commander of the U.S. Fleet. In 1939, Kirk became the American naval attaché in London, where he familiarized himself thoroughly with Royal Navy practices—practices he strongly admired, even though British condescension occasionally irked him. His forceful advocacy of greater Anglo-American cooperation and his urgent warnings in 1940 of the extreme danger Britain faced helped persuade President Franklin D. Roosevelt and his administration to assist Britain with measures potentially liable to precipitate conflict with Germany.
In March 1941, Kirk became director of Naval Intelligence, but partially because of fierce bureaucratic infighting with the War Plans Division, his office failed to produce any specific warnings of Japan's intentions vis-à-vis the United States, despite clues that an attack on American forces was being planned. In October 1941, he returned to sea duty as commander of a division of destroyer escorts in the Atlantic Fleet, fortuitously escaping responsibility for the failure to predict the Pearl Harbor raid.
Promoted to rear admiral in November 1941, Kirk became chief of staff to Admiral Harold Stark, commander of American naval forces in Europe, in March 1942. In London, he contributed substantially to Allied strategic planning. In February 1943, Kirk took command of Amphibious Force, Atlantic Fleet, and that July, he led an amphibious naval task force in the Sicily landings. His outstanding success in the face of unexpectedly difficult conditions brought him command of all U.S. naval forces for the June 1944 Normandy landings. Later that year, he commanded all U.S. naval forces in France. He was promoted to vice admiral in May 1945.
Kirk retired with the rank of admiral in March 1946. He then served as ambassador to Belgium and minister to Luxembourg until 1949 and spent a further two years as ambassador to the Soviet Union (April 1949 to October 1951) and the Republic of China (May 1962 to April 1963). Kirk died in New York City on 15 October 1963.
Belot, Raymond de. The Struggle for the Mediterranean, 1939–1945. Princeton, NJ: Princeton University Press, 1951.; Dorwart, Jeffery. Conflict of Duty: The U.S. Navy's Intelligence Dilemma, 1919–1945. Annapolis, MD: Naval Institute Press, 1983.; Jones, Matthew. Britain, the United States, and the Mediterranean War, 1942–1944. New York: St. Martin's Press, 1996.; Leutze, James R. Bargaining for Supremacy: Anglo-American Naval Collaboration, 1937–1941. Chapel Hill: University of North Carolina Press, 1977.; Morison, Samuel Eliot. History of United States Naval Operations in World War II. Vol. 5, The Struggle for Guadalcanal, August 1942–February 1943. Boston: Little, Brown, 1949.; Morison, Samuel Eliot. History of United States Naval Operations in World War II. Vol. 11, The Invasion of France and Germany, 1944–1945. Boston: Little, Brown, 1957.