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, Ayanami was assigned to Destroyer Division 19 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.

On 19 December, Ayanami sank the Dutch submarine HNLMS O 20 with assistance from her sister ships Uranami and Yugiri and rescued 32 survivors.

[8][page needed] Ayanami subsequently was part of the escort for the heavy cruisers Suzuya, Kumano, Mogami and Mikuma in support of "Operation L" (the invasion of Banka, Palembang and the Anambas Islands in the Netherlands East Indies), taking minor damage after striking a reef in the Anambas, necessitating a return to Camranh Bay, French Indochina for emergency repairs.

[10] Ayanami sailed from Amami-Ōshima to Mako Guard District, Singapore, Sabang and Mergui for a projected second Indian Ocean raid.

[11][page needed] Ayanami's final mission, on November 14–15, 1942, was that of the Second Naval Battle of Guadalcanal, where she was conducting transport runs.

Thirty surviving crew members including Commander Sakuma escaped in a boat to Guadalcanal; the remainder were taken off by Uranami.

[13] In late July 1992 marine archeologist Robert Ballard led an expedition to Ironbottom Sound, finding thirteen newly discovered shipwrecks.