As it was formed in part from reservists and cadre that included members of the Communist Party from that city, it carried the honorific title "Rostov" for the duration.

[1] Its primary order of battle was as follows: Col. Aleksandr Mikhailovich Pykhtin took command of the division on the day it began forming, a position he would hold until December 15.

In the following days the 339th, along with its companion divisions and 16th Rifle Brigade, was ordered to defend its namesake city by the Army commander, Maj. Gen. Viktor Tsyganov, by manning the outer and inner defensive belts on the northern and eastern sectors.

56th Army was forced to withdraw as well, and after a bitter defense mainly by NKVD security troops Rostov-on-Don fell to the Germans for the second time on July 27.

Its V Army Corps broke into the city on August 10, but a spirited defense of the suburb of Pashkovskaya by 30th Rifle allowed most of the defenders to evacuate south of the Kuban River before the bridge was blown up in the Germans' faces, further delaying their advance.

Leaving the reserves in July, it returned to 56th Army in the revived North Caucasus Front and fought on the Taman Peninsula from August to November under the 16th Rifle Corps.

At 1325 hours on November 16 the German air force began a series of heavy strikes against the division's positions, with over 100 Ju 87 and Bf 109 sorties.

Colonel Kulakov had established his observation post in the midst of his division's forward defense line in the northern portion of the Voikov factory.

Unaware of his fate, the People's Commissariat of Defense issued a decree the following day promoting Kulakov to the rank of Major General.

On May 16, 1944, Kulakov was posthumously made a Hero of the Soviet Union for his outstanding performance in the Kerch–Eltigen Operation, along with a captain and a sergeant-major of his division who were also killed during its course.

On November 15 a new Separate Coastal Army was formed from the command elements of North Caucasus Front, and 16th Rifle Corps was assigned to it.

On the night of January 22–23, Army commander Col. Gen. Ivan Petrov ordered a coup de main against Kerch, with the Azov Flotilla transporting two naval infantry battalions into the harbor.

The picture changed by the 21st, as 16th Corps continued attacking to the northwest and completed the breakthrough of the main German defensive zone, reaching as far as the Oder–Spree Canal.