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, Amagiri 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.

From 4 December 1941, to the end of the year, Amagiri covered the landings of Japanese troops in Malaya, and was part of the escort in support of "Operation L" (the invasion of Banka and Palembang in the Netherlands East Indies.

[7] On 4–5 June, Amagiri participated in the Battle of Midway as part of the Aleutian Invasion force and was subsequently based at Amami-Ōshima for patrols of southern waters until mid-July.

During this operation, she was attacked 60 nmi (110 km; 69 mi) north-northeast of Savo Island by United States Marine Corps SBD Dauntless dive bombers from Henderson Field, which sank her sister ship Asagiri and severely damaged Shirakumo.

On 5–6 July, during the Battle of Kula Gulf Amagiri was engaged by United States Navy destroyers and cruisers while attempting a troop transport mission to Kolombangara.

On 2 August, while returning from another "Tokyo Express" night reinforcement fast transport mission to Vila, Amagiri rammed and sank the US torpedo boat PT-109, commanded by Lieutenant, junior grade (and future US president) John F. Kennedy.

However, Robert J. Donovan in his book PT 109: John F. Kennedy in WWII, after interviewing many of the crew, concludes that it was not an accident, and he talked to the man at the wheel who was ordered to steer for a collision course.

The incident would be publicized in several books, a movie, and a hit song by Jimmy Dean, as "the Jap destroyer in the night, cut the 109 in two", making it probably the only Japanese ship to ever be mentioned in the top ten of the Billboard Hot 100 singles charts.

Sent back to Kure Naval Arsenal for repairs in January 1944, she was reassigned to the Southwest Area Fleet in March and was based in Singapore to provide escort for transport missions in the western Netherlands East Indies.