Pierre Konowaloff, a naturalised Frenchman, claims that Van Gogh's Night Cafe, which has hung on the walls of Yale University for nearly 50 years, was confiscated from his great-grandfather Ivan Morozov on the orders of Lenin.
A court ruling in his favour would trigger a flood of similar claims from Russian émigrés whose family art collections were plundered by the Bolshevik government.
Mr Konowaloff's lawyer, Allan Gerson, has argued that the confiscation of all privately held art in Russia after the revolution was no different to the looting of the Nazis, who are believed to have plundered 20 per cent of Western Europe's art.
"I contend that there is no difference," Mr Gerson said.
After Mr Konowaloff's lawyers wrote to Yale demanding the painting's surrender, the university was forced to file suit in a U.S. court to resolve the issue of ownership.
Regarded as one of the artist's most profound interpretations of the human condition, Night Cafe was bequeathed to Yale in 1960 by Stephen Clark, a collector and benefactor who attended the university.
It was originally sold to a Berlin art gallery as one of dozens of masterpieces offloaded by Stalin in the early 1930s to finance a five-year plan meant to modernise Soviet industry and agriculture.
Yale maintains that the sale was legal and cannot therefore be challenged.
"There is no wrong to be addressed," the university writes in its affidavit. "It was accepted at the time, as it is now, that the sale by the Soviet government was valid, as were later acquisitions of the panting."
Mr Konowaloff says he intends to give the painting to the Russian state in exchange for unspecified financial compensation.
His previous campaigns to claim ownership of other paintings have caused alarm in Russia, which remains the main beneficiary of the confiscation of Morozov's collection, considered one of the finest in private hands before the revolution.
A critically acclaimed exhibition of Russian art at the Royal Academy was nearly called off last year after Mr Konowaloff claimed ownership of some of the exhibits. The dispute was only resolved when parliament rushed through legislation to guarantee that the art could not be seized.
The issue of plundered art remains controversial. The debate was renewed in January when Sir Norman Rosenthal, a luminary of the art establishment, voiced his opposition to the return of Nazi art plunder to the descendants of the original owners.
Much of the missing art stolen by the Nazis was subsequently looted by the Red Army and secretly hidden in Russia for 50 years. Although Russia pledged to begin returning it in the 1990s, the process has stalled since Vladimir Putin came to power in 2000.