That spring, Whippoorwill operated with Canopus (AS-9) during maneuvers in the southern Philippines, touching at Zamboanga and steaming in the Sulu Sea, before returning to Cavite and anchoring in Canacao Bay.

Whippoorwill operated on patrol duties and laid mines—laying the field near Caballo Island, near Corregidor, at the entrance to Manila Bay.

Relieved by Tulsa on station on 30 November, Whippoorwill returned to Canacao Bay before she got underway on 3 December for sweeping operations out of Cavite.

In the ensuing action, Whippoorwill claimed assists in splashing two bombers and sending another one crashing on shore nearby.

Ferriter saw Peary's predicament and moved his ship through the burning navy yard and eased Whippoorwill near the destroyer's stern and passed a towline.

Braving the burning firebrands from the blazing warehouse, the destroyermen made fast the line, and the minesweeper commenced backing.

Finally, on the third try, the line held; and, with debris showering upon the minesweeper and her crippled charge, Whippoorwill pulled Peary free.

Soon thereafter, Whippoorwill moored Peary to a buoy in Manila Bay and took the destroyer's wounded to the hospital at Sangley Point in her motor launch.

Three days later, the minesweeper commenced local patrols and sweeps out of Surabaya and continued that duty into February 1942, often operating in company with Dutch units, before she received orders to move to Tjilatjap, a port on Java's south coast.

Arriving early on 26 February, Whippoorwill and Lark put to sea at 1400 the next day to search for survivors of the seaplane tender Langley (AV-3), reportedly sunk south of Java.

At 2229, Whippoorwill and Lark arrived in the area in which Langley had been reported lost, passed a large oil slick, and smelled a strong odor of gasoline and oil—mute testimony to the tragedy that had gone before.

Ten injured men were transferred to Tulsa, which had also arrived on the scene of the rescue—the gunboat having a well-equipped sick bay that the minesweepers lacked.

Following that rescue mission, Whippoorwill returned to Tjilatjap, arriving on 1 March, only to stand out later that day as Java, too, was becoming more untenable with each passing hour.

The minesweeper conducted local patrols and guardship operations in the shipping channels and harbors there from mid-May to late August when she returned to Fremantle.

For the remainder of 1942, Whippoorwill operated alternatively at Exmouth Bay, Albany, or Fremantle, patrolling locally and towing targets.

The beginning of 1943 found Whippoorwill engaged in local patrol operations out of Exmouth Gulf, and she continued that duty until February, when she made another brief visit to Fremantle.

Coming under the operational control of Commander, Service Force, 7th Fleet, Whippoorwill arrived at Brisbane on 20 March.

She then continued operations off New Guinea and in the backwater areas of the war in the Pacific until receiving orders to head north for Leyte in February 1945.

Arriving there on 5 February 1946, Whippoorwill soon began preparation for inactivation and, on 17 April 1946, the ship was decommissioned at San Francisco, California.