After the Munich Agreement, the Soviet Union pursued a rapprochement with Nazi Germany. On 23 August 1939, the Soviet Union signed a non-aggression pact with Germany which included a secret protocol that divided Eastern Europe into German and Soviet spheres of influence, anticipating potential "territorial and political rearrangements" of these countries. Germany invaded Poland on 1 September 1939, starting World War II. The Soviets invaded eastern Poland on 17 September. Following the Winter War with Finland, the Soviets were ceded territories by Finland. This was followed by annexations of the Baltic states and parts of Romania.

On 22 June 1941, Adolf Hitler launched Operation Barbarossa, an invasion of the Soviet Union with the largest invasion force in history, resulting in large battles and horrific atrocities. This offensive comprised three army groups. The city of Leningrad was besieged while other major cities fell to the Germans. Despite initial successes, the German offensive ground to a halt in the Battle of Moscow, and the Soviets launched a counteroffensive, pushing the Germans back. The failure of Operation Barbarossa reversed the fortunes of Germany, and Stalin was confident that the Allied war machine would eventually defeat Germany. The Soviet Union repulsed Axis attacks, such as in the Battle of Stalingrad and the Battle of Kursk, which marked a turning point in the war. The Western Allies provided support to the Soviets in the form of Lend-Lease as well as air and naval support. Stalin met with Winston Churchill and Franklin D. Roosevelt at the Tehran Conference and discussed a two-front war against Germany and the future of Europe after the war. The Soviets launched successful offensives to regain territorial losses and began a push to Berlin. The Germans unconditionally surrendered in May 1945 after Berlin fell.

The bulk of Soviet fighting took place on the Eastern Front—including the Continuation War with Finland—but it also invaded Iran in August 1941 with the British. The Soviets later entered the war against Japan in August 1945, which began with an invasion of Manchuria. They had border conflicts with Japan up to 1939 before signing a non-aggression pact in 1941. Stalin had agreed with the Western Allies to enter the war against Japan at the Tehran Conference in 1943 and at the Yalta Conference in February 1945 once Germany was defeated. The entry of the Soviet Union in the war against Japan along with the atomic bombings by the United States led to Japan's surrender, marking the end of World War II. During the war, the Soviet Union, along with the United States, the United Kingdom and China, were considered the Big Four of Allied powers.

The Soviet Union suffered the greatest number of casualties in the war, losing more than 20 million citizens, about a third of all World War II casualties. The full demographic loss to the Soviet people was even greater. The German Generalplan Ost aimed to create more Lebensraum (lit. 'living space') for Germany through extermination. An estimated 3.5 million Soviet prisoners of war died in German captivity as a result of deliberate mistreatment and atrocities, and millions of civilians, including Soviet Jews, were killed in the Holocaust. However, at the cost of a large sacrifice, the Soviet Union emerged as a global superpower. The Soviets installed dependent communist governments in Eastern Europe, and tensions with the United States and the Western allies grew to what became known as the Cold War.

During the 1930s, Soviet foreign minister Maxim Litvinov emerged as a leading voice for the official Soviet policy of collective security with the Western powers against Nazi Germany. In 1935, Litvinov negotiated treaties of mutual assistance with France and with Czechoslovakia with the aim of containing Hitler's expansion. After the Munich Agreement, which gave parts of Czechoslovakia to Nazi Germany, the Western democracies' policy of appeasement led the Soviet Union to reorient its foreign policy towards a rapprochement with Germany. On 3 May 1939, Stalin replaced Litvinov, who was closely identified with the anti-German position, with Vyacheslav Molotov.

In August 1939, Stalin accepted Hitler's proposal of a non-aggression pact with Germany, negotiated by foreign ministers Vyacheslav Molotov for the Soviets and Joachim von Ribbentrop for the Germans. Although officially a non-aggression treaty only, an appended secret protocol, also reached on 23 August, divided the whole of eastern Europe into German and Soviet spheres of influence. The USSR was promised the eastern part of Poland, then primarily populated by Ukrainians and Belarusians, in case of its dissolution, and Germany recognised Latvia, Estonia and Finland as parts of the Soviet sphere of influence, with Lithuania added in a second secret protocol in September 1939. Another clause of the treaty was that Bessarabia, then part of Romania, was to be joined to the Moldovan SSR, and become the Moldovan SSR under control of Moscow.

The pact was reached two days after the breakdown of Soviet military talks with British and French representatives in August 1939 over a potential Franco-Anglo-Soviet alliance. Political discussions had been suspended on 2 August, when Molotov stated that they could not be resumed until progress was made in military talks late in August, after the talks had stalled over guarantees for the Baltic states, while the military talks upon which Molotov insisted started on 11 August. At the same time, Germany, with whom the Soviets had started secret negotiations on 29 July argued that it could offer the Soviets better terms than Britain and France, with Ribbentrop insisting "there was no problem between the Baltic and the Black Sea that could not be solved between the two of us." German officials stated that, unlike Britain, Germany could permit the Soviets to continue their developments unmolested, and that "there is one common element in the ideology of Germany, Italy and the Soviet Union: opposition to the capitalist democracies of the West". By that time, Molotov had obtained information regarding Anglo-German negotiations and a pessimistic report from the Soviet ambassador in France.

After disagreement regarding Stalin's demand to move Red Army troops through Poland and Romania (which Poland and Romania opposed), on 21 August, the Soviets proposed adjournment of military talks using the pretext that the absence of senior Soviet personnel at the talks interfered with the autumn manoeuvres of the Soviet forces, though the primary reason was the progress being made in the Soviet-German negotiations. That same day, Stalin received assurance that Germany would approve secret protocols to the proposed non-aggression pact that would grant the Soviets land in Poland, the Baltic states, Finland and Romania,. Stalin telegrammed Hitler that night that the Soviets were willing to sign the pact and that he would receive Ribbentrop on 23 August. Regarding the larger issue of collective security, some historians believe that one reason that Stalin decided to abandon the doctrine was the shaping of his views of France and Britain by their entry into the Munich Agreement and the subsequent failure to prevent the German occupation of Czechoslovakia. Stalin may also have viewed the pact as a way of gaining time in an eventual war with Hitler in order to reinforce the Soviet military and shifting Soviet borders westwards, which would be militarily beneficial in such a war.