Vereshchagin graduated first in his list at the naval school, but left the service immediately to begin the study of drawing in earnest. Two years later, in 1863, he won a medal from the St Petersburg Academy for his Ulysses Slaying the Suitors. In 1864, he proceeded to Paris, where he studied under Jean-Léon Gérôme, though he dissented widely from his master's methods.
In 1871, Vereshchagin established an atelier in Munich. He gave a solo exhibition of his works (later referred to as his "Turkestan Series") at the Crystal Palace in London in 1873. He gave another exhibition of his works in St Petersburg in 1874, where two of his paintings, namely, The Apotheosis of War, dedicated "to all conquerors, past, present and to come," and Left Behind, the picture of a dying soldier deserted by his fellows, were denied a showing on the grounds that they portrayed the Russian military in a poor light.
In late 1874, Vereshchagin departed for an extensive tour of the Himalayas, India and Tibet, spending over two years in travel. He returned to Paris in late 1876.
Vereshchagin painted several scenes of imperial rule in British India. His epic portrayal of The State Procession of the Prince of Wales into Jaipur in 1876 is said to be the third largest painting in the world. In 1882–1883, he again traveled to India. He aroused much controversy by his series of three pictures: firstly, of a Roman execution (the Crucifixion by the Romans (1887)); secondly, Suppression of the Indian Revolt by the English; and, thirdly, of the execution of Nihilists in St Petersburg. His picture Suppression of the Indian Revolt by the English depicted executions of sepoys carried out by tying victims to the barrels of guns. Vereshchagin's detractors argued that such executions had only occurred in the Indian Rebellion of 1857, but the painting depicted modern soldiers of the 1880s, implying that the practice was then current. Because of its photographic style, the painting appeared to present itself as an impartial record of a real event. In 1887 Vereshchagin defended himself in The Magazine of Art by saying that if there were another rebellion then the British would use this method again.
By the late 19th century, Vereshchagin had gained popularity, not only in Russia, but also abroad and his name never left the pages of the European and American press. From his earliest works, unlike most contemporary battle pieces depicting war as a kind of parade, Vereshchagin graphically depicted the horrors of war. "I loved the sun all my life, and wanted to paint sunshine. When I happened to see warfare and say what I thought about it, I rejoiced that I would be able to devote myself to the sun once again. But the fury of war continued to pursue me". Vereshchagin wrote. One day, in 1882, Vereshchagin's exhibition in Berlin was visited by German field marshal Helmuth von Moltke the Elder. Vereshchagin brought Moltke to his painting The Apotheosis of War. The picture evoked a sort of confusion in the field marshal. After his visit to the exhibition, Moltke issued an order forbidding German soldiers to visit it. The Austrian war minister did the same. He also declined the artist's offer to let Austrian officers see his pictures free of charge at the 1881 exhibition in Vienna.
In Russia, a ban on exhibitions of Vereshchagin's work was also enforced, as well as a ban on reproductions of them in books and periodicals amidst accusations of slandering the Russian army. The artist took these unjust accusations badly and burned three of his paintings, The Forgotten Soldier, They Have Encircled, and Pursue and They Entered.
A journey in Syria and Palestine in 1884 furnished him with an equally discussed set of subjects from the New Testament. Vereshchagin's paintings caused controversy over his portrayal of the figure of Christ with what was thought at the time to be an unseemly realism. His depiction of Jesus's features was thought to be excessively vulgar and over-emphatically Semitic in ethnicity.
The "1812" series on Napoleon's Russian campaign, on which Vereshchagin also wrote a book, seems to have been inspired by Tolstoi's War and Peace, and was painted in 1893 in Moscow, where the artist eventually settled.
During the Russo-Japanese War, he was invited by Admiral Stepan Makarov to join him aboard Makarov's battleship, Petropavlovsk. On April 13, 1904, Petropavlovsk struck two mines while returning to Port Arthur and sank, taking with it most of the crew, including both Admiral Makarov and Vereshchagin. Vereshchagin's last work, a picture of a council of war presided over by Admiral Makarov, was recovered almost undamaged.