Dmitry Ivanovich Donskoy was born in 1350. After his father's death in 1359, nine-year-old Prince Dmitry came under the guardianship of Metropolitan Alexius, who became the de facto ruler of the Moscow principality due to his authority and strong character. Ivan the Red bequeathed his possessions, inherited from Ivan Kalita, to his sons Semyon and Dmitry. After the quick death of his younger brother, all these lands came under Dmitry's control.

In the Golden Horde, after the death of Berdibek, a power struggle began, known as the "great turmoil." After the death of Ivan the Red, the Grand Duchy of Vladimir was transferred to the Nizhny Novgorod-Suzdal princes. In 1362, the temnik Mamai, who effectively ruled on behalf of Khan Abdullah, issued a charter to Dmitry Ivanovich, and the Moscow army expelled Dmitry Konstantinovich from Pereyaslavl and Vladimir. Subsequently, Moscow supported his claims to Nizhny Novgorod in exchange for renouncing claims to Vladimir, and Dmitry Ivanovich married his daughter Evdokia.

The disintegration of the Golden Horde affected not only its Asian part: Tagai strengthened in the Mordovian lands, and Bulat-Timur in Volga Bulgaria. Both were defeated: by the Ryazanians in 1365 and by the Suzdalites in 1367. In 1370, the Suzdalites invaded Volga Bulgaria, placing Mamai's appointees there, which expanded his influence over lands west of the Volga.

In 1362, the Grand Duke of Lithuania, Olgerd, defeated three Tatar princes at the Blue Waters, annexing Kiev, Podolia, and other lands to his state, freeing them from dependence on the Horde. In 1368, the conflict in the Tver principality escalated, where Mikhail Alexandrovich took the Tver throne with Olgerd's support, ousting Vasily Mikhailovich. Moscow invaded Tver twice, while Olgerd unsuccessfully besieged Moscow, where a new white-stone Kremlin was built in 1367.

By the early 1370s, the southern Russian lands that were part of the Grand Duchy of Lithuania renewed their tribute dependence within the Lithuanian-Tatar alliance against Moscow. For participating in Olgerd's second campaign against Moscow, Metropolitan Alexius excommunicated the Smolensk prince Svyatoslav Ivanovich from the church. In 1371, Olgerd appealed to the Patriarch of Constantinople to appoint a separate metropolitan in Kiev.

In 1370, Mamai issued a charter to Mikhail of Tver, who began active military actions in Northeastern Russia. Dmitry gathered troops and refused to comply with Mamai's demands. In 1371, Dmitry concluded an agreement with Mamai, establishing a lower tribute and redeeming the Tver prince's son. Olgerd moved against Moscow for the third time, but the Lyubut peace was concluded.

In 1371, Dmitry attempted to control Ryazan, but in 1372, Oleg returned. In 1373, Mamai attacked Ryazan, but in 1374, Dmitry established a "rozmirie" with him, which meant the cessation of tribute payments. In 1374, a congress of princes took place in Pereyaslavl-Zalessky, aimed at consolidating anti-Horde forces around Moscow.

In 1376, Dmitry sent troops to Volga Bulgaria, and in 1377, the Moscow-Suzdal army was destroyed by the Tatars. In 1378, the Tatar tumens were defeated at the River Vozha. That same year, Metropolitan Alexius died, and Dmitry tried to appoint his confessor to the metropolitan throne.

In 1379, Mamai again devastated the Ryazan principality. In 1380, Mamai launched a campaign against Moscow, but Dmitry refused to pay tribute and led his troops to meet him. After the victory at Kulikovo Field, Dmitry did not continue the campaign deeper into the steppes. Mamai was defeated by Tokhtamysh, and Dmitry concluded peace with Tokhtamysh, retaining the Vladimir charter.

In 1382, Tokhtamysh captured Moscow, but Dmitry made an agreement with him, retaining the Vladimir charter. In 1384, a preliminary marriage agreement was made between Yagailo and Dmitry's daughter, but Yagailo chose Catholicism and concluded a union with Poland.

In 1386, Dmitry received tribute from Novgorod after attacks by the ushkuiniks. In 1388, a conflict arose with Vladimir Andreyevich over the question of the throne's inheritance, but Dmitry managed to reconcile with him before his death on May 19, 1389.

In his will, Dmitry mentioned the grand duchy and other lands, stating that minor princes should live in Moscow. However, the will contained ambiguities, which were later used in the struggle for the throne.

Dmitry Donskoy became a recognized leader of anti-Horde policy, strengthening the Moscow principality and expanding its territory. However, western lands were lost, and the territory was ravaged by wars and invasions. Monastery-fortresses were built in Moscow, and silver coin minting began. Dmitry Ivanovich Donskoy died on May 19, 1389, and was buried in the Archangel Cathedral of the Kremlin.