Cherokee Guns shared an image of the sign, which features the faces of Alexandria Ocasio-Cortez, Ilhan Omar, Ayanna Pressley and Rashida Tlaib accompanied by the caption: “The Four Horsemen are Idiots”.
The North Carolina gun shop’s advert is signed by “the Deplorables”.
The billboard has been condemned by the congresswomen pictured as well as anti-gun violence advocates.
“How the hell is this not inciting violence?” Ms Tlaib tweeted on Wednesday evening.
The Coalition to Stop Gun Violence called the billboard “violent rhetoric”.
“Threats against members of Congress, particularly minority members are [trending upward] and it is driven by the president's racial rhetoric,” the group wrote. “This is dangerous!!!”
Ms Pressley told congressman Mark Meadows, whose district houses the shop, to “do the right thing.”
It comes after the US president told the four Democratic congresswomen, who are all US citizens, to “go back” to the countries they came from in a series of racist tweets last month.
Earlier this year, a New York man was arrested and charged with threatening to kill Ms Omar in a phone call to her Washington office.
“Do you work for the Muslim Brotherhood?” authorities say the man asked the staffer who answered the phone. “Why are you working for her, she's a [expletive] terrorist. I'll put a bullet in her [expletive] skull.”
Days later, President Donald Trump tweeted a video juxtaposing Ms Omar with footage of the twin towers falling on 9/11.
The post triggered a flood of threatening messages so severe that Democratic leaders increased the congresswoman's security, and an independent cybersecurity executive took it upon himself to flag them for the social network's monitors.
Last week, two Louisiana police officers were fired for a Facebook post that suggested Ms Ocasio-Cortez should be shot.
The congresswoman blamed Mr Trump’s rhetoric for the deluge of threats she and her colleagues had received.
“This is Trump's goal when he uses targeted language & threatens elected officials who don't agree w/ his political agenda,” she wrote on Twitter.
“It's authoritarian behaviour. The President is sowing violence. He's creating an environment where people can get hurt & he claims plausible deniability.”
As people flocked to Cherokee Gun's Facebook page Monday, the group put out a statement indicating they'd received “OVERWHELMING demand” for items with the billboard's image.
“Alright my fellow Infidels for Trump... due to OVERWHELMING demand... you may come by the shop (next week) and get your very own FOUR HORSEMEN COMETH STICKER...simple...eat a piece of bacon...tell us you're voting for Trump in 2020... then get your limited edition bumper sticker! (While supplies last!) Snowflakes and Liberals are not eligible... sorry...”
Cherokee Guns has a long history of controversial billboards, especially ones that are overtly Islamophobic.
In 2017, the store posted a picture of another sign with “a great message”. “INFIDEL ARMAMENT” it read in block letters above Arabic script and a rifle.
Two years before that, the shop put up a billboard that said, “Give me your tired, your poor... Keep your Syrian refugees”, the Asheville Citizen Times reported.
This week, the Citizen Times reported that it spoke to the store's owner, Doc Wacholz, who downplayed his billboard's implications and sought to justify its message.
“They're socialists, from my point of view,” he told the local paper, before adding: “I also feel a couple of them, being Muslim, have ties to actual terrorists groups.”
“I'm not inciting any violence or being racist,” he added. “It's a statement. It's an opinion.”
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