She put to sea on 1 April 1940 for fleet exercises in the Hawaiian area, followed by overhaul at Mare Island Navy Yard at Vallejo, California.

Upon completion, Stingray returned to the Hawaiian area, where she remained until joining the Asiatic Fleet at Cavite, Philippine Islands, on 23 October 1941.

Stingray was at Manila on 7 December during the Japanese attack on Pearl Harbor, and immediately put to sea on her first war patrol.

She fired four torpedoes at the first ship, and the resultant explosion quickly sank the converted gunboat Saikyo Maru.

On 23 August 1943, Stingray departed Brisbane for her ninth war patrol, conducted en route to Pearl Harbor.

On 31 August, a United States Army Air Forces B-24 Liberator bomber attacked her as she crash-dived in the Solomon Sea 30 nautical miles (56 km; 35 mi) west of Buka Island at 05°24′S 154°07′E / 5.400°S 154.117°E / -5.400; 154.117, dropping three 500-pound (227 kg) bombs which missed her by 50 feet (15 m)..[5] Stingray suffered significant damage but no casualties.

Following return to Pearl Harbor, Stingray got underway on 10 March 1944 for her tenth war patrol conducted in the Mariana Islands.

Inasmuch as the submarine was in the middle of the ocean, with her charts showing over 2,000 fathoms (12,000 ft; 3,700 m) of water, the first thoughts of the commanding officer concerned what new type of antisubmarine measure the enemy was using.

For her twelfth war patrol, Stingray carried out a special mission, landing fifteen Filipino officers and men and six tons of supplies on the northeastern coast of Luzon.

On the way back to Port Darwin, Australia, on 18 August, she picked up four Japanese sailors from the cruiser Natori, which was sunk earlier in the day.

Stingray was underway again on 10 September 1944 for her thirteenth war patrol, spent on a special mission to look over possible landing beaches at Marjoe Island.

She was on the surface in the Pacific Ocean 100 nautical miles (185 km; 115 mi) east-northeast of Morotai at 02°45′S 129°52′E / 2.750°S 129.867°E / -2.750; 129.867 on 3 October 1944 when a U.S. Navy TBF Avenger torpedo bomber from the escort carrier USS Midway (CVE-63) mistakenly attacked her.

She returned to Fremantle, Western Australia, on 23 February and then headed back to the United States arriving at New London, Connecticut, on 29 April.