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Dmitry Ivanovich, later known as Dmitry Donskoy, was born in Moscow in 1350, the son of Ivan II Ivanovich, Prince of Moscow and Grand Prince of Vladimir, and Alexandra Vasilyevna Velyaminova. When Ivan II died in 1359, Dmitry, then a child of about nine years, succeeded as Prince of Moscow. During his minority the affairs of the principality were guided by Metropolitan Alexius, who acted as regent and worked to preserve Moscow's position among the northeastern Russian lands. In the early 1360s Dmitry received from the Khan of the Golden Horde the yarlyk conferring the title of Grand Prince of Vladimir, the traditional senior dignity among the princes of Rus'. Rival claimants, especially the princes of Tver, contested this status, and Dmitry's early reign was occupied with wars and negotiations that gradually confirmed Moscow's precedence.

In the later 1360s Dmitry undertook the rebuilding of Moscow's fortifications in stone, replacing earlier wooden walls. The white-stone Kremlin begun around 1367 became a symbol of Muscovite strength and helped the city withstand a Lithuanian siege in 1368. He fought repeated campaigns against Grand Prince Mikhail of Tver and against Algirdas of Lithuania, who intervened in Russian affairs, and also came into conflict with Oleg of Ryazan. These struggles, together with shifting alliances among the Russian principalities, formed the political background to his later confrontation with the Golden Horde. Throughout this period Moscow remained a tributary of the Horde, but Dmitry increasingly acted as a leader of a coalition of princes rather than as a purely subordinate vassal.

The decisive military episode of his reign was the campaign of 1380 against Mamai, a powerful emir who controlled the western part of the Golden Horde. After Mamai formed an alliance with Lithuania and demanded increased tribute, Dmitry gathered forces from Moscow and allied principalities and met Mamai's army on 8 September 1380 at Kulikovo Field, near the upper Don. The Russian victory earned Dmitry the epithet Donskoy. Traditional accounts associate the opening of the battle with a single combat involving the monastic warrior Alexander Peresvet. The triumph was short-lived in political terms: in 1382 Khan Tokhtamysh, who had reunited much of the Horde, sacked Moscow after a siege, and Dmitry was obliged to resume tribute. Nonetheless, Kulikovo entered Russian historical memory as a turning point in the long process of emancipation from Mongol overlordship and as a demonstration of Moscow's claim to lead the Russian lands.

In 1366 Dmitry married Eudoxia Dmitriyevna, daughter of Dmitry Konstantinovich, Prince of Suzdal and Nizhny Novgorod. The marriage sealed a political alliance and produced a large family. Their eldest surviving son, Vasily, succeeded Dmitry as Grand Prince (Vasily I). Other sons included Yury of Zvenigorod, Andrey of Mozhaysk, Peter of Dmitrov, and Konstantin; daughters were married into other princely houses. Dmitry died in Moscow on 19 May 1389, still in his late thirties, and was buried in the Cathedral of the Archangel in the Moscow Kremlin, the traditional necropolis of the Muscovite dynasty. In his last will he treated the Grand Principality of Vladimir as a hereditary possession of his line, to be passed to Vasily without a new grant from the khan, an important assertion of dynastic right.

The Russian Orthodox Church numbered Dmitry among the saints at the Local Council of 1988, held in the year of the millennium of the Baptism of Rus'. He is commemorated on 19 May, the day of his death. His widow Eudoxia later took the monastic name Euphrosyne and was herself glorified as a saint. In church and national tradition Dmitry Donskoy is remembered as a pious ruler, a builder of Moscow, and a defender of the Orthodox faith against both internal rivals and the Horde. Historians generally regard his reign as a crucial stage in the rise of Moscow as the political center of the northeastern Russian principalities, even though Mongol suzerainty was not yet overthrown.

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