Following his education at the Imperial Academy of Arts in Saint Petersburg, Aivazovsky traveled to Europe and lived briefly in Italy in the early 1840s.

[18] In 1833, Aivazovsky arrived in the Russian capital, Saint Petersburg, to study at the Imperial Academy of Arts in Maxim Vorobiev's landscape class.

[14][22] In 1839, he took part in military exercises in the shores of Crimea, where he met Russian admirals Mikhail Lazarev, Pavel Nakhimov and Vladimir Kornilov.

[23][22] He first traveled to Venice via Berlin and Vienna and visited San Lazzaro degli Armeni, where an important Armenian Catholic congregation was located and his brother Gabriel lived at the time.

[24] Upon his return to Russia, Aivazovsky was made an academician of the Imperial Academy of Arts and was appointed the "official artist of the Russian Navy to paint seascapes, coastal scenes and naval battles.

"[19][22] In 1845, Aivazovsky traveled to the Aegean Sea with Duke Konstantin Nikolayevich and visited the Ottoman capital, Constantinople, and the Greek islands of Patmos and Rhodes.

[25][26] Aivazovsky held an 1881 exhibition at London's Pall Mall, attended by English painter John Everett Millais and Edward VII, Prince of Wales.

The next year, the 50th anniversary of his creative labors, was celebrated with an exhibition in St Petersburg, and an honorary membership in the Imperial Academy of Fine Arts.

In him alone there are combined a general, a bishop, an artist, an Armenian, an naive old peasant, and an Othello.After traveling to Paris with his wife, in October 1892 he made a trip to the United States, visiting Niagara Falls in New York and Washington D.C.[26][36][37] During this trip, he performed an act of diplomacy by donating to the Corcoran Museum two of his paintings, which he had painted in "Russia, Crimea, Feodosia", Relief Ship (Russian: Корабль помощи) and Food Distribution (Russian: Раздача продовольствия) which commemorated the arrival of American aid to Russia during the Tsar's famine of 1891-1892 but the Tsar barred these paintings in Russia because of their anti-monarchist unpatriotic themes.

[46] A quote from Movses Khorenatsi's History of Armenia in Classical Armenian is engraved on his tombstone: Mahkanatsu tsneal anmah ziurn yishatak yetogh (Մահկանացու ծնեալ անմահ զիւրն յիշատակ եթող),[47] which translates: "He was born a mortal, left an immortal legacy"[45] or "Born as a mortal, left the immortal memory of himself".

Among the most notable were held in Rome, Naples and Venice (1841–42), Paris (1843, 1890), Amsterdam (1844), Moscow (1848, 1851, 1886), Sevastopol (1854), Tiflis (1868), Florence (1874), St. Petersburg (1875, 1877, 1886, 1891), Frankfurt (1879), Stuttgart (1879), London (1881), Berlin (1885, 1890), Warsaw (1885), Constantinople (1888), New York (1893), Chicago (1893), San Francisco (1893).

[19] Classic painters like Salvator Rosa, Jacob Isaacksz van Ruisdael and Claude Lorrain contributed to Aivazovsky's individual process and style.

[9] Karl Bryullov, best known for his The Last Day of Pompeii, "played an important part in stimulating Aivazovsky's own creative development," according to Bolton.

"[54] She, like most scholars, considered his Ninth Wave his best piece of art and argued that it "seems to mark the transition between fantastic color of his earlier works, and the more truthful vision of the later years.

[9] The distinct transition in Russian art from Romanticism to Realism in the mid-nineteenth century left Aivazovsky, who would always retain a Romantic style, open to criticism.

Proposed reasons for his unwillingness or inability to change began with his location; Feodosia was a remote town in the huge Russian empire, far from Moscow and Saint Petersburg.

He depicted "the romantic struggle between man and the elements in the form of the sea (The Rainbow, 1873), and so-called "blue marines" (The Bay of Naples in Early Morning, 1897, Disaster, 1898) and urban landscapes (Moonlit Night on the Bosphorus, 1894).

[63] His other themed works from this period include rare portraits of notable Armenians, such as his brother Archbishop Gabriel Aivazovsky (1882), Count Mikhail Loris-Melikov (1888), Catholicos Mkrtich Khrimian (1895), Nakhichevan-on-Don Mayor Аrutyun Khalabyan and others.

[66] In 1871 he founded the construction of a new Museum of Antiquities on Mount Mitridat modeled after a typical Ancient Greek temple of the Doric order.

[69] A 1903 encyclopedic article stated: "Although Kuindzhi cannot be called a student of Aivazovsky, the latter had without doubt some influence on him in the first period of his activity; from whom he borrowed much in the manner of painting.

"[70] English art historian John E. Bowlt wrote that "the elemental sense of light and form associated with Aivazovsky's sunsets, storms, and surging oceans permanently influenced the young Kuindzhi.

[25] The prominent Armenian poet Hovhannes Tumanyan wrote a short poem titled "In Front of an Aiazovsky painting" in 1893, inspired by a seascape.

[116] In 2007, when Abdullah Gül became president of Turkey, he brought paintings by Aivazovsky up from the basement to hang in his office during redecoration of the presidential palace, the Çankaya Mansion in Ankara.

[122] Works by Aivazovsky, among others, are presumed to have been destroyed in an airstrike attack on the Kuindzhi Art Museum in Mariupol during the Russian invasion of Ukraine in March 2022.

[123] According to Ukrainian authorities, Russian forces looted a number of original works by Aivazovsky from Mariupol museums to Russian-controlled Donetsk.

[148] In early March 2023, the Metropolitan Museum of Art changed Aivazovsky's label to "Armenian, born Russian Empire [now Ukraine].

[151] The Soviet Union (1950), Romania (1971),[152] Armenia (first in 1992),[153] Russia (first in 1995),[154] Ukraine (1999),[155] and other countries have issued postage stamps depicting Aivazovsky or his works.

An exhibition featuring 120 paintings and 55 etchings of Aivazovsky was held at the Tretyakov Gallery on Krymsky Val in Moscow from 29 July to 20 November 2016 dedicated to his 200th anniversary of birth.

[171] In January 2011 a number of paintings, including those of Aivazovsky, were stolen from the country house of Aleksandr Tarantsev, an owner of a chain of jewelry stores in Russia, outside Moscow.

[172][173] In 2017 it was reported that a fake of one of the paintings stolen from Tarantsev's house was presented to Armenian president Serzh Sargsyan by the Pyunik foundation.