Dargomyzhsky grew up in St. Petersburg as a talented amateur musician, playing the violin and piano and dabbling in composition. His acquaintance with the composer Mikhail Glinka (Glinka, Mikhail) (1833) turned his thoughts more seriously toward composition, and in 1839 he completed his first opera, Esmeralda (after Victor Hugo (Hugo, Victor); performed 1847). Two other operas followed: The Triumph of Bacchus (1845; performed 1867) and Rusalka (after Aleksandr Pushkin (Pushkin, Aleksandr Sergeyevich); produced 1856). In his songs Dargomyzhsky developed an individual vein of humour and satire. His orchestral pieces (e.g., Finnish Fantasia, Cossack Dance, and Baba-Yaga) were notable for their harmonic experiments.

After 1866 he became interested in developing a Russian national music of great dramatic realism and began to set Pushkin's play Kamennygost (The Stone Guest) to a species of melodically heightened recitative, with entire passages composed in the whole-tone (whole-tone scale) mode. This work aroused the interest of Mily Balakirev (Balakirev, Mily) and his circle, particularly Modest Mussorgsky (Mussorgsky, Modest); when Dargomyzhsky died, the score was completed by César Cui (Cui, César) and orchestrated by Nikolay Rimsky-Korsakov (Rimsky-Korsakov, Nikolay).