1940, Aylwin, as a unit of the "maroon" fleet, participated in Fleet Problem XXI, the last pre-war fleet problem. Indicative of the Fleet's security-mindedness at that time, Aylwin alternated with other destroyers conducting "security patrols" off the port of Honolulu and off Pearl Harbor's entrance during the course of the evolutions, investigating all vessels sighted, including small fishing craft. Detachments from the Fleet were rotated back to the west coast at intervals. Aylwin thus returned briefly to the west coast during the summer of 1940, reaching San Diego on 9 July before shifting to the Mare Island Navy Yard on the 14th. She underwent repairs and alterations there until 22 September before returning, via San Diego, to Pearl Harbor on 21 October. 1941 From that port, Aylwin maintained her normal routine into the critical year 1941. On 7 February 1941, she put to sea and, after rendezvousing with aircraft carrier Enterprise and sister destroyer , headed back to the west coast for a brief visit. They arrived at San Diego on 13 February, but turned around again two days later and rejoined Enterprise—which was ferrying a shipment of the latest Army fighter aircraft to Hawaii. The three ships reached Oahu on 21 February. On 17 March, Aylwin left Pearl Harbor for off-shore patrol and exercises. Two days later, the ship conducted a two-hour night tactical exercise on a dark, moonless night, commencing at 20:00. At its conclusion, all destroyers were directed to proceed to a rendezvous astern of the fleet's center. At 22:51, Aylwin turned on her running and fighting lights and sighted a ship materializing out of the murk on her port bow. Aylwin maintained her course and speed until backing emergency full at 23:03. At that point, the other ship, Farragut, loomed on a collision course and also backed to avoid contact. Shortly after 23:04, Farraguts bow sliced into Aylwins port side at a 90-degree angle, causing extensive damage for about 23 frames and nearly severing Aylwin'''s bow. A fire immediately blazed up as high as Aylwins masthead, illuminating the two ships and quickly spread aft through the wardroom and into the area occupied by the ships officers' cabins. Aylwin's electrical installation burned with intense heat until controlled at 0140 on the 20th. Fire parties from Dale, , , and all contributed men to help contain the blaze; and a party from Indianapolis joined the one from Philadelphia