Ray Albers had been with the police department in nearby St. Ann, Mo., for 20 years. He quit Thursday after the board of police commissioners recommended termination or resignation.
The Glendale, Mo., department fired another officer, Matthew Pappert, for his criticism of the protesters on Facebook. Pappert was suspended last week.
Pappert later apologized for his "insensitive" posts. He suggested protesters should be "put down like rabid dogs," and called them "a burden on society and a blight on the community."
Albers was captured on video by witnesses who saw him raise a gun in a confrontation with protesters. The video posted on Youtube shows that when someone asked his name, he responded "Go f---- yourself."
St. Ann Police Chief Aaron Jiminez said he believed Albers was justified in raising his rifle because he had seen a man with a gun in the crowd and heard gunshots from another direction. Jiminez suggested his comment was a result of being under pressure.
"I'm not condoning his behavior whatsoever," Jiminez said Thursday. "It's very hard because he is a good friend, he was a good boss. There's going to be those who didn't like him who are high-fiving now. Altogether it's going to be a black eye on the city of St. Ann because he represented our department."