She screened Wasp as the aircraft carrier launched air strikes supporting the Marines in the initial days of this long and bitter struggle, and acted as flagship for Destroyer Squadron 12.

Back at Espiritu Santo on 6 October 1942, she joined a force whose mission was to intercept and destroy Japanese shipping and to prevent the reinforcement of Guadalcanal by the nightly Tokyo Express runs into the island.

On 13 May she drove off a bomber attack which wounded one of her men, and on 30 June engaged shore batteries on the coast of New Georgia at Munda to protect transports landing troops on the island of Rendova across the channel.

As the New Georgia operation continued, with new landings at various points on the large island, Farenholt escorted support shipping north from the lower Solomons and fired shore bombardment until 16 July 1943.

After a brief period alongside a tender at Espiritu Santo, she operated out of that port and Efate on escort and patrol duty between Nouméa and Guadalcanal, sweeping against Japanese shipping, and bringing troops and supplies to Vella Lavella.

On the night of 17/18 February, her squadron made a daring dash down St. George Channel to fire on shipping in Blanche Bay and bombard Rabaul, sinking two merchantmen and inflicting much damage on shore installations.

Farenholt's squadron, however, was detached to meet with Canberra and Houston, damaged in the air battles off Taiwan earlier in the month and still making their retirement toward Ulithi.

She sailed north to San Pedro Bay, arriving 19 June, to join the logistics group supporting the fast carriers in their air strikes against the Japanese home islands.

On 28 July, Farenholt returned to Okinawa for screening duties until 22 September, when she sailed with an Army general aboard to accept the Japanese surrender of islands in the southern Ryukyus and in the Sakishima Gunto.