Vsevolod Pudovkin was born in Penza into a Russian family, the third of six children. His father Illarion Epifanovich Pudovkin came from peasants of the Penza Governorate, the village of Shuksha and worked in several companies as a manager and a door-to-door salesman. Vsevolod's mother Elizaveta Alexandrovna Pudovkina (née Shilkina) was a housewife.
A student of engineering at Moscow University, Pudovkin saw active duty during World War I, being captured by the Germans. During this time he studied foreign languages and did book illustrations. After the war, he abandoned his professional activity and joined the world of cinema, first as a screenwriter, actor and art director, and then as an assistant director to Lev Kuleshov.
His first notable work was a comedy short Chess Fever (1925) co-directed with Nikolai Shpikovsky. José Raúl Capablanca played a small part in it, with a number of other cameos presented. In 1926 he directed which will be considered one of the masterpieces of silent movies: Mother, where he developed several montage theories that would make him famous. Both movies featured Pudovkin's wife Anna Nikolaevna Zemtsova in the main female parts (she left cinema shortly after).
His first feature was followed by The End of St. Petersburg (1927), and Storm Over Asia (also known as The Heir of Genghis Khan), titles which compose a trilogy at the service of the bolshevik revolutionary policy.
In 1928, with the advent of sound film, Pudovkin, Sergei Eisenstein and Grigori Aleksandrov signed the Manifest of Sound, in which the possibilities of sound are debated, and always understood as a complement to image. This idea would be brought to bear in his next pictures: A Simple Case (1932) and The Deserter (1933), works that do not match the quality of earlier work. In 1935 he was awarded the Order of Lenin.
After an interruption caused by health concerns, Pudovkin returned to movie making, this time with a number of historical epics: Victory (1938); Minin and Pozharsky (1939) and Suvorov (1941). The last two were often praised as some of the best movies based on Russian history, along with the works of Sergei Eisenstein. Pudovkin was awarded a Stalin Prize for both of them in 1941.
During World War II he was evacuated to Kazakhstan where he directed several patriotic war movies. He also played a small part in the Ivan the Terrible movie (as God's fool). With the end of war he returned to Moscow and continued his work at the Mosfilm studio, making biographical and war movies. In 1947 he was awarded another Stalin Prize for his work on Admiral Nakhimov, and in 1950 — his second Order of Lenin and a third Stalin Prize for Zhukovsky. His last work was The Return of Vasili Bortnikov (1953).