Eaker remained with the 64th Infantry until March 1918, when he was placed on detached service to receive flying instruction at Austin and Kelly Fields in Texas. Upon graduation the following October, he was rated a pilot and assigned to Rockwell Field, California.
In July 1919, he transferred to the Philippine Islands, where he served with the 2d Aero Squadron at Fort Mills until September 1919; with the 3d Aero Squadron at Camp Stotsenburg until September 1920, and as executive officer of the Department Air Office, Department and Assistant Department Air Officer, Philippine Department, and in command of the Philippine Air Depot at Manila until September 1921.
Meanwhile, on July 1, 1920, he was commissioned into the Regular Army as a captain in the Air Service and returned to the United States in January 1922, for duty at Mitchel Field, New York, where he commanded the 5th Aero Squadron and later was post adjutant.
In June 1924, Eaker was named executive assistant in the Office of Air Service at Washington, D.C., and from December 21, 1926, to May 2, 1927, he served as a pilot of one of the Loening OA-1 float planes of the Pan American Goodwill Flight that made a 22,000 mile (35,200 km) trip around South America and, with the others, was awarded the Mackay Trophy. He then became executive officer in the Office of the Assistant Secretary of War at Washington, D.C.
In September 1926, he was named operations and line maintenance officer at Bolling Field, Washington, D.C. While on that duty, he participated as chief pilot on the endurance flight of the Army plane, Question Mark, from 1 to January 7, 1929, establishing a new world flight endurance record. For this achievement the entire crew of five, including Eaker and mission commander Major Carl Spaatz, were awarded the DFC. In 1930, he made the first transcontinental flight entirely with instruments.
In October 1934, Eaker was ordered to duty at March Field, Calif., where he commanded the 34th Pursuit Squadron and later the 17th Pursuit Squadron. In the summer of 1935, he was detached for duty with the Navy and participated aboard the aircraft carrier USS Lexington, on maneuvers in Hawaii and Guam.
Eaker entered the Air Corps Tactical School at Maxwell Field, Alabama, in August 1935, and upon graduation the following June entered the Command and General Staff School at Fort Leavenworth, Kansas, from which he graduated in June 1937. During his time at Ft Leavenworth from June 3–7, 1936, Eaker made the first blind (instruments only) transcontinental flight from New York to Los Angeles. He then became assistant chief of the Information Division in the Office of the Chief of Air Corps (OCAC) at Washington, D.C., during which he helped plan and publicize the interception of the Italian liner Rex at sea. In November 1940, Eaker was given command of the 20th Pursuit Group at Hamilton Field, California. Promoted in 1941 to colonel while at Hamilton Field.