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By 1935 Beria was one of Stalin's most trusted subordinates. He cemented his place in Stalin's entourage with a lengthy oration "On the History of the Bolshevik Organisations in Transcaucasia" (later published as a book), which rewrote the history of Transcaucasian Bolshevism emphasizing Stalins's role in it. When Stalin's purge of the Communist Party and government began in 1934 after the assassination of Sergei Kirov, Beria ran the purges in Transcaucasia, using the opportunity to settle many old scores in the politically turbulent Transcaucasian republics. In June 1937 he said in a speech: "Let our enemies know that anyone who attempts to raise a hand against the will of our people, against the will of the party of Lenin and Stalin, will be mercilessly crushed and destroyed".

Beria at the NKVD

An official poster eulogising BeriaIn August 1938 Stalin brought Beria to Moscow as deputy head of the People's Commissariat for Internal Affairs (NKVD), the ministry which oversaw the state security and police forces. Under Nikolai Yezhov, the NKVD carried out prosecution of the perceived enemies of the state known as the Great Purge, that affected millions of people. By 1938, however, the purge had become so extensive that it was damaging the infrastructure of the Soviet state, its economy and armed forces, and Stalin had decided to wind the purge down. In September Beria was appointed head of the Main Administration of State Security (GUGB) of the NKVD, and in November he succeeded Yezhov as head of NKVD (Yezhov was executed in 1940). The NKVD itself was then purged, with half its personnel replaced by Beria loyalists, many of them from the Caucasus.

Beria's name has become closely identified with the Great Purge as well, but in fact he presided over the NKVD during an easing of the repression. Over 100,000 people were released from the labour camps, and it was officially admitted that there had been some injustices and "excesses" during the purges, which were blamed on Yezhov. Nevertheless this liberalisation was only relative: arrests and executions continued, and in 1940, as war approached, the pace of the purges again accelerated. During this period Beria supervised the deportations of population from Poland and the Baltic states following their occupation by Soviet forces.

In March 1939 Beria became a candidate member of the Communist Party's Politburo. Although he did not become a full member until 1946, he was already one of the senior leaders of the Soviet state. In 1941 Beria was made a Commissar General of State Security, a highest military-like rank within the Soviet police ranking system of that time.

In February 1941 he became a Deputy Chairman of the Council of People's Commissars (Sovnarkom), and in June, when Nazi Germany invaded the Soviet Union, he became a member of the State Defence Committee (GKO). During World War II he took on major domestic responsibilities, using the millions of people imprisoned in NKVD labour camps for wartime production. He took control of production of armaments and (with Georgy Malenkov) aircraft and aircraft engines. This was the beginning of Beria's alliance with Malenkov, which later became of central importance.

In 1944, as the Germans were driven from Soviet soil, Beria was in charge of dealing with the various ethnic minorities accused of collaboration with the invaders, including the Chechens, the Ingush, the Crimean Tatars and the Volga Germans. All these were deported to Soviet Central Asia. See "Population transfer in the Soviet Union".

In December 1944 Beria was also charged with supervision of the Soviet atomic bomb project. In this connection he ran the successful Soviet espionage campaign against United States atomic weapons programme which resulted in Soviets obtaining a nuclear bomb technology, building and testing a bomb in 1949.