In 1916, at the age of 16 and after completing his junior year in high school, he was appointed to the United States Naval Academy at Annapolis in Maryland, along the Chesapeake Bay.

Cunningham was commissioned an ensign in the United States Navy and his first assignment was on the naval transport USS Martha Washington, which brought troops home from France.

His command briefing gave top priority to completing the naval air station, over any attention to improving the island's defenses.

On December 8, 1941, news of the attack on Pearl Harbor naval / air bases in Hawaii reached Wake Island at 07:00 am, less than 2+1⁄2 hours after the Japanese struck further east.

Cunningham recalled the Philippine Clipper (a Martin 130 flying boat) of Pan American Airways and set in motion plans for a scouting patrol.

Cunningham ordered the Marine commander, Major James Devereux, to hold their fire until the ships were in easy range.

The small U.S. force on the island repulsed the initial landing attempt, but they were in serious need of additional supplies and support – including gunsights, spare parts and fire-control radar – which Cunningham had requested earlier from the commandant, 14th Naval District.

Cunningham and his fellow prisoners were taken aboard the Japanese transport Nitta Maru to Shanghai, China by way of Yokohama, Japan.

On September 10, 1945, Cunningham underwent a complete physical examination at the National Naval Medical Center in Bethesda, Maryland.

In January 1946, he began a period of retraining, beginning with refresher aviation training at the Naval Air Station in Pensacola, Florida.

During his time as commander, Curtiss operated with patrol squadrons in the Formosa Strait, ferried men and supplies to outlying bases and made several visits to Qingdao, China, before returning the United States in March 1947.