Construction of the advanced Fubuki-class destroyers was authorized as part of the Imperial Japanese Navy's expansion program from fiscal 1923, intended to give Japan a qualitative edge with the world's most modern ships.

At the time of the attack on Pearl Harbor, Asagiri was assigned to Destroyer Division 20 of Desron 3 of the IJN 1st Fleet, and had deployed from Kure Naval District to the port of Samah on Hainan Island, escorting Japanese troopships for landing operations in the Battle of Malaya.

[6][7][page needed] Asagiri subsequently was part of the escort for the heavy cruisers Suzuya, Kumano, Mogami and Mikuma in support of the "Operation L" (the invasion of Banka and Palembang and the Anambas Islands in the Netherlands East Indies).

During this operation, she took a direct hit from a bomb dropped from torpedo launchers by United States Marine Corps SBD Dauntless dive bombers from Henderson Field.

The explosion killed 122 men, including 60 ground troops, and sank Asagiri near Santa Isabel, 60 nautical miles (110 km) north-northeast of Savo Island at position 08°0′S 160°10′E / 8.000°S 160.167°E / -8.000; 160.167.