Pyryev was born in Kamen-na-Obi, Altai Krai, Russia. His early career included acting on stage directed by Vsevolod Meyerhold in The Forest («Лес») and by Sergei Eisenstein in the Proletcult Theatre production The Mexican. Pyryev also acted in Eisenstein's first short film Glumov's Diary. Pyryev's early career included production jobs behind the camera, such as work for director Yuri Tarich. He débuted as a director in the age of silent film, with Strange Woman (Посторонняя женщина, 1929).
During the 1930s and 1940s Pyryev rivaled Grigori Aleksandrov as the country's most successful director of musical comedies, all of which starred his wife Marina Ladynina. Even during wartime, when the Soviet film industry had been evacuated to Alma-Ata, Pyryev made popular and light-hearted features. In Six O'Clock after the War is Over the Romantic characters (played by Ladynina and Yevgeny Samoilov), when separated by war, arrange a date at 6 PM on the Victory Day, and the victory celebrations are shown towards the end of the film (which was released in November 1944).
Such films as They Met in Moscow (1941), Ballad of Siberia (1947) and Cossacks of the Kuban (1949) have often been broadcast on national television and proved effective in showcasing the idealized Soviet way of life. The former, shown in the US as They Met in Moscow, was the last film made in the Soviet Union before the German invasion. The protagonists, a Russian swineherd and a Chechen shepherd (played by Ladynina and Vladimir Zeldin) meet at the All-Union Agricultural Exhibition and fall in love with each other. The movie is noted for a memorable score by Isaak Dunaevsky and Tikhon Khrennikov. Cossacks of the Kuban, which launched the star of Klara Luchko, presents a highly glamorized picture of life in a southern kolkhoz.
Following Joseph Stalin's death, Pyryev turned his attention to adaptations. He produced two acclaimed adaptations of Fyodor Dostoevsky's novels, The Idiot (1958, starring Yuri Yakovlev) and The Brothers Karamazov (1969), which was nominated for the Academy Award for Best Foreign Language Film and won him a Special Prize at the 6th Moscow International Film Festival. Pyryev died at the age of 66 in Moscow. Since The Brothers Karamazov was unfinished at the time, the film stars Kirill Lavrov and Mikhail Ulyanov are usually credited with having brought the project to a conclusion. His widow Lionella Pyryeva, who took the part of Grushenka in The Brothers Karamazov, went on to marry Oleg Strizhenov.
Grigori Roshal wrote that "Pyriev's comedies speak of man's right to happiness, the attainment of which, in his native country, is not hindered by any national or class distinctions."