The new vessel was laid down in October 1934, and launched eighteen months later. DD-379 was commissioned exactly two years, to the day, after her keel-laying ceremony took place. Briefly, after her shakedown, USS PRESTON operated under the control of the Chief of Naval Operations for evaluation purposes and special training "evolutions", then was assigned first to DESRON 2 and subsequently to DESRON 5.

December 7, 1941 found DD-379 on patrol and coastal escort duties along the West Coast, where she would remain well into the summer of 1942. As the operations in the Pacific accelerated, USS PRESTON was transferred west to meet with her new charge, the large carrier, USS SARATOGA (CV-3). The destroyer would support vessels replenishing the carriers after the pivotal Battle of Midway, but operations quickly shifted to the south, and DD-379 moved toward the action. On October 24, 1942, USS PRESTON, along with the other destroyers screening the carriers of TASK FORCE 61, deployed to defend the flat tops from a massive air strike. The battle, which would be named for the Santa Cruz Islands proved a bloody one for both the Japanese and the Americans. DD-379 was able to shoot down two attackers.

The Naval Battle of Guadalcanal
Following a short resupply trip to Noumea, the destroyer was immediately in the thick of action again. Allied coast watchers and reconnaissance flights confirmed a strong Japanese force was steaming down "the Slot", a strait between the almost parallel lines of islands in the Solomons, leading from Bougainville to Guadalcanal. The Imperial Japanese Navy intended to blast the American airfield on "the Canal", named Henderson Field, with heavy weapons, then to devastate the beachhead. A huge battleship, IJN KIRISHIMA, two heavy cruisers, two light cruisers, and nine destroyers, under the command of VADM Hiroaki Abe, were assigned the task. In support were two carriers, two more battleships, two cruisers, and more than a dozen destroyers.

To meet the enemy force, RADM Willis Augustus Lee deployed two battleships and four destroyers. The American force steamed east around Savo Island, unaware in the gloom of the night, that they had been sighted and were being followed into Ironbottom Sound by the Japanese force. Abe split the Japanese force into four elements, convinced that his ships faced only a small cruiser-destroyer force. Prior to midnight, the big American battleship USS WASHINGTON (BB-56) fired the first rounds of the Naval Battle of Guadalcanal at the Japanese cruiser IJN SENDAI. From that point, the opposing forces swept by each other on almost reciprocal courses and blasted away with guns and torpedoes.

The first mortal wound was suffered by USS PRESTON. Unseen by the American destroyers, the Japanese cruiser IJN NAGARA and her two-destroyer escort had slipped into the Sound just South of Savo Island. The enemy force ambushed the American destroyers at almost point-blank range. The American destroyer USS WALKE (DD-416) fired first, to be answered by a torrent of 6-inch shells from the Japanese cruiser. USS WALKE, USS BENHAM (DD-397), and USS PRESTON were all hit, but DD-379 was hit hardest. In less than ten minutes, USS PRESTON was a floating pyre. Her bridge wrecked, after stack trailing over the side, and both fire rooms demolished, the destroyer drew fire from most of the Japanese forces in the Sound as they rushed past to slug it out with Lee's battleships. Settling by the stern, the gallant destroyer rolled over on her port side and sank.117 of the crew died and 147 survived though 31 were wounded. The survivors were rescued by the USS Meade and amongst those lost was the Commanding Officer Cmdr Max Clifford Stormes.

The Naval Battle of Guadalcanal was hailed as a victory for the Americans. At the cost of three destroyers, RADM Lee destroyed a battleship and a destroyer. More importantly, the massive effort to destroy the American beachhead on Guadalcanal and devastate Henderson Field had been blocked. The Americans were on the island to stay. The great advance on Japan had begun. USS PRESTON had not died in vain. For her actions in World War II, USS PRESTON earned two battle stars.