They have swamped social media with an image of a rifle-carrying Jihadi and a bomb bearing the regime’s infamous black flag.
It stands in front of Volgograd Arena in Southern Russia football stadium.
An official symbol of the finals is also included in the alarming promise to bring mayhem to the tournament.
The 2018 FIFA World Cup will be played across 11 cities in Russia from 14 June to 15 July, when the final will be played at the Luzhniki Stadium in Moscow.
Tens of thousands of England fans are expected to base themselves in St Petersburg for the month-long finals.
Russia’s second largest city was scene of an horrific ISIS attack when a briefcase bomb detonated on the underground in April, killing 14 people.
The blast was in retaliation to Russia’s airstrikes in Syria that have helped bring the regime to its knees.
Last week ISIS released another propaganda image featuring bullet-ridden photos of President Donald Trump and Russian President Vladimir Putin, inviting its followers to stage more attacks on the group's two leading foes abroad.
The image, shared throughout pro-ISIS channels on the encrypted messaging application Telegram, featured an excerpt of a Quranic verse manipulated by the ISIS followers to urge fellow jihadis to take every opportunity to conduct deadly attacks in the U.S. and Russia.
Despite the jihadis suffering severe territorial losses to military campaigns sponsored by Moscow and Washington, the image also claimed that ISIS would overcome its enemies on the battlefield.
"Lie in wait for them at every chance to ambush," the text reads beneath photos of Trump and Putin pasted to gun target practice sheets. "The Levant is the graveyard of the Russians and Americans."
Thousands of Russians from mainly central Asia have travelled to the Middle East to fight for ISIS. Experts in Moscow believe around 2,400 joined the regime in 2015 alone.
Islamic extremism is a concern for Putin, said Ian Brzezinski, senior fellow at the Atlantic Council.
"Despite his government's defence doctrines stating that the US and NATO is Russia's greatest threat, I have always felt that Putin regards Islamic extremism to be the most immediate threat," Brzezinski said.
"Putin cut his teeth destroying the Chechens.
"He regarded their rebellion as a manifestation of Islamic extremism.
"He also bolstered his own personal popularity in Russia by demonising the Chechens as Islamic terrorists and by brutally crushing them."