Dmitry Venevitinov was born on September 14, 1805, in Moscow, in the parish of the now non-existent church of Archdeacon Eupolis, which was located at the intersection of Myasnitskaya Street and Milyutinsky Lane. His father, Vladimir Petrovich Venevitinov, a former ensign of the Semenovsky Regiment, came from a wealthy noble family in Voronezh. His mother, Anna Nikolaevna, was from the princely Obolensky-Belye family, and through her, Dmitry was distantly related to A. S. Pushkin, being his fourth cousin.

Venevitinov grew up in a house on Krivokolenny Lane, where he received a classical home education under the guidance of his mother. He was taught French and Latin, as well as classical literature, by the governor d'Orrier, a former French officer. Greek was taught by a Greek named Beyla, painting by the artist Lapersh. Venevitinov studied Russian literature with Professor A. F. Merzlyakov at Moscow University, and music, probably with I. I. Genishta. He also mastered German well, presumably with the help of H. I. Gerke, the governor of his deceased brother Peter.

In 1822, Dmitry Venevitinov became a student at Moscow University, where he became interested in German philosophy and romantic poetry. He attended lectures, including courses by A. F. Merzlyakov, I. I. Davydov, M. G. Pavlov, and Loder. In 1823, he successfully passed his exams and in 1824 began working at the Moscow Archive of the Ministry of Foreign Affairs, which Pushkin ironically referred to as "the archive youths" in "Eugene Onegin." In August and September 1824, he visited his estates in Voronezh with his younger brother Alexei, which was reflected in his letters.

Venevitinov, along with Prince V. F. Odoevsky, founded a secret philosophical "Society of Lovers of Wisdom," which included I. V. Kireevsky, A. I. Koshelev, V. P. Titov, N. A. Melgunov, and others. The circle also included M. P. Pogodin and S. P. Shevyrev. The group studied German idealist philosophy, the works of Friedrich Schelling, Immanuel Kant, Fichte, Oken, Friedrich Schlegel, and others. Venevitinov actively participated in the publication of the journal "Moscow Herald."

In November 1826, thanks to the patronage of Princess Zinaida Volkonskaya, Venevitinov moved from Moscow to St. Petersburg, where he began working in the Asian Department of the Ministry of Foreign Affairs. Upon entering St. Petersburg, he was arrested on suspicion of involvement in the Decembrist conspiracy while accompanying the wife of Decembrist Prince S. P. Trubetskoy, Ekaterina Ivanovna. He spent three days in custody and was interrogated by the duty general of the Main Headquarters, A. N. Potapov. According to biographers, the arrest and interrogation had a significant impact on Venevitinov. In St. Petersburg, he lived in the house of the Lansky family, where he felt oppressed by being away from his family and friends, despite a wide circle of acquaintances, including V. F. Odoevsky and A. I. Koshelev. A. Delvig was a frequent guest.

On March 2, Venevitinov caught a severe cold while running from a ball at the Lansky house to his wing, and on March 15, 1827, he died in St. Petersburg, likely from severe pneumonia, not reaching the age of 22. He was buried in the Church of St. Nicholas by the Sea, and his body was sent to Moscow, where he was interred at the cemetery of the Simonov Monastery. A. Pushkin and A. Mickiewicz attended the funeral.

Venevitinov bequeathed to have a ring made of Herculaneum, a gift from Zinaida Volkonskaya, placed on his finger at the moment of his death. When he fell into unconsciousness, A. S. Khomyakov put the ring on his finger, and when Venevitinov regained consciousness, he asked, "Are they marrying me?" After that, he died.

In the 1930s, during the demolition of the Simonov Monastery, Venevitinov's remains were exhumed and reburied at Novodevichy Cemetery. The remains of his mother and brother Alexei were not reburied; their graves were destroyed. The ring was removed from the poet's finger by the wife of architect Peter Baranovsky, Maria Yuryevna, and is kept in the Literary Museum.

In his literary activity, Venevitinov displayed diverse talents and interests. He was not only a poet but also a prose writer, wrote literary-programmatic and critical articles, and engaged in polemics with N. A. Polevoy regarding the first chapter of Pushkin's "Eugene Onegin," translating works by German authors, including Goethe and Hoffmann. Venevitinov wrote about 50 poems, many of which, especially the later ones, are filled with deep philosophical meaning, which is a distinctive feature of his lyrics.