Post-war
Ingalls returned to Yale and received an LLD from Harvard in 1923. After graduating, he joined Squire, Sanders & Dempsey as an associate. In 1926, he was elected to the Ohio General Assembly, where he co-sponsored the Ohio Aviation Code. Ingalls also served as a member of the Ohio House of Representatives from 1927 to 1929. He was a good friend of Jack Towers, who recommended Ingalls for the job of Assistant Secretary of the Navy (AIR). He asked Newton Baker, a friend of his father to recommend him to Herbert Hoover. He got the job in early 1929. He became a good friend of Hoover, who invited him to the White House and to his camp. Fellow Skull and Bones member F. Trubee Davison would often accompany them. On his way home in his plane from Washington in June 1929, Ingalls crashed his plane into a fence, but was unharmed. As Assistant Secretary, he tripled the number of naval aircraft and pushed for a fully deployable carrier task force. In 1932, he embarked on an unsuccessful campaign to become Governor of Ohio. He left in 1933 to become director of Cleveland's Department of Public Health and Welfare.
In the mid-1930s, Ingalls was appointed a lieutenant commander in the Naval Reserves. He was made vice president and general manager of Pan Am Air Ferries in 1941. After the attack on Pearl Harbor by the Japanese, he helped develop the Naval Air Station at Honolulu, and ended up reporting for duty. In 1943, he became Chief of Staff for the Forward Area Air Center Command and later Commander of the Pearl Harbor Naval Air Station.
On his return to Ohio, he became a director of Pan Am World Airways and managed Robert A. Taft's campaign to be the Republican nominee for president in 1952. In 1954, he became president and publisher of the Cincinnati Times-Star and Vice Chairman of the now defunct Taft Broadcasting Company. He left the Cincinnati Times-Star in 1958 to practice law.
Ingalls was a friend of the aviator Charles Lindbergh, whom he helped solve navigation and communication problems in charting new air routes to the east for Pan Am.
He was a director of the Cleveland Trust Company, director of South Eleuthera Properties, Vice President of Virginia Hot Springs, Inc., President of the Central Eyebank for Sight Restoration, trustee of Laurel School and an honorary trustee of the Young Men's Christian Association.