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Commissioned with Captain Yokokawa Ichibei in command only three months before the Pearl Harbor attack, fleet carrier Zuikaku nevertheless participated in the attack that started the Pacific War. During the Pearl Harbor attack, the first wave of 30 aircraft launched from her flight deck attacked Wheeler Field and Naval Air Station at Kaneohe, while the second wave of 44 aircraft attacked Hickam Field and battleships California and Maryland. The attack was a stunning success, and the pilots returned as heroes.

On 20 Jan 1942, Zuikaku's aircraft attacked Rabaul. On 21 Jan, they attacked Lae, New Guinea. In Apr 1942, she was a member of the task force that ventured into the Indian Ocean and struck the British naval bases at Ceylon.

In May 1942, Zuikaku participated in Operation MO, which was the invasion plan of Port Moresby. The Japanese signals were intercepted and decrypted by Allied intelligence, and carriers Yorktown and Lexington were dispatched. The ensuing Battle of the Coral Sea cost her half of her aircraft, while her sister ship Shokaku was heavily damaged by three bombs. As a result, both carriers were unable to participate in the Battle of Midway in the following month, where the presence of these two additional fleet carriers could have resulted in a much different outcome.

Under the command of Captain Tameteru Notomo, Zuikaku sailed for the Solomon Islands in Aug 1942. During the Battle of the Eastern Solomons on 24 Aug 1942, light carrier Ryujo acted as bait to draw the attention of American aircraft, therefore allowed aircraft from Zuikaku and Shokaku to attack American fleet carriers. Zuikaku's aircraft heavily damaged Enterprise with several 1,000-lb bombs, but Enterprise's effective damage control kept the American carrier from becoming disabled. Enterprise was sidelined for repairs for three months after the battle.

In Feb 1943, Zuikaku and her aircraft covered the evacuation of Guadalcanal. Later that year, Captain Kikuchi Tomozo took over command of the carrier and countered American naval forces in the Marshall Islands area.

In Jun 1944, Zuikaku participated in Operation A-Go which led to the Battle of Philippine Sea. At the end of the battle, 429 Japanese aircraft were destroyed, along with the destruction of Taiho and Shokaku by submarines. Zuikaku was now the last surviving carrier of the Pearl Harbor attack.

In Oct 1944, Zuikaku was Admiral Jisaburo Ozawa's flagship for the decoy fleet that successfully lured away Admiral William Halsey's fleet, therefore allowing the Battle off Samar to take place. On 24 Oct 1944, Halsey caught up with Ozawa. Zuikaku was struck by seven torpedoes and nine bombs and was abandoned at 1358 that day. She rolled over and sank at 1414. Captain Kaizuka Takeo and 842 men went down with her.

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