In a video posted to the influential lobby's Twitter account, spokesperson Dana Loesch accused critics of trying to undermine the former real estate mogul's presidency.
"We are witnesses to the most ruthless attack on a president and the people who voted for him, and the free system that allowed it to happen, in American history," she announces at the start of the video.
Ms Loesch continues to accuse "saboteurs" of targeting the Trump administration with "leaks and smears".
"From the highest levels of government, to their media, universities and billionaires, their hateful defiance of his legitimacy is an insult to each of us,” she says.
Menacingly, she adds: "The ultimate insult is that they think we're so stupid that we'll let them get away with it."
She also accuses critics of trying to "drive their daggers through the heart of [America's] future", as images of NFL players kneeling appear on screen.
The video ends with the line: "We are the National Rifle Association of America. And we are freedom's safest place."
This is not the first time the NRA has come under fire for releasing incendiary content.
In April, Ms Loesch said anti-Trump sentiment was "the violence of lies", that should be countered with the "clenched fist of truth."
In August, she told the New York Times, "we're coming for you."
"We're going to laser-focus on your so-called 'honest pursuit of truth.' In short, we're coming for you," she said. "Consider this a shot across your proverbial bow."