Chief Tim Gannon and Officer Kim Potter quit the Brooklyn Center force on Tuesday.
The pair said she shot Daunte Wright accidentally, having mistakenly drawn her gun instead of her Taser.
The death happened in a suburb of Minneapolis, a city already on edge amid the trial of an ex-police officer accused of murdering George Floyd.
On Tuesday night bottles and other projectiles were thrown at police headquarters and officers responded by firing tear gas, stun grenades and rubber bullets.
More than 60 people were arrested, Minnesota State Patrol Colonel Matt Langer told
Another demonstration broke out over the killing in Portland, Oregon on Tuesday night, with about 100 protesters marching on the Portland Police Association Building.
Flames were seen coming out of the side of the police building about an hour later. The Portland Police Bureau declared the gathering a riot.
Portland was the centre of mass demonstrations last year, in the wake of the killing of George Floyd.
Speaking to reporters earlier, Brooklyn Center Mayor Mike Elliott said that he had appointed 19-year veteran Tony Gruenig to take over for Tim Gannon.
On Monday, Mr Gannon had said that the shooting of Mr Wright appeared to be an "accidental discharge" after Mrs Potter mistook her service pistol for a stun gun.
"I appreciate the officer stepping down," the mayor said, adding that he hoped her leaving would "bring some calm to the community".
He said the city had intended to fire Mrs Potter. "We want to send a message to the community that we are taking this situation seriously," he added.
Meanwhile prosecutors are expected to decide whether to charge Mrs Potter on Wednesday, the Associated Press reported.
"We have to make sure that justice is served, justice is done. Daunte Wright deserves that. His family deserves that," Mr Elliott said.
Standing outside the Brooklyn Center police department, she described how upset she had been with the actions of the police.
"She should have been fired," said Ms Young, referring to the police officer. "Her resignation should not have come before [that]."
When it comes to the police chief, she said simply: "I'm glad he's gone. He showed no concern for the community."
She was one of the few protesters at the police department on Tuesday, standing in the wind, as ice and rain whipped around her.
The police officers who were guarding the premises had also dwindled. After a moment, Ms Young herself turned around to leave. Still, she said she would return at night.
Like many of those who have come here to express their anger at the police, she is determined to get her message across. For them, the departures of the police officer and the chief are an important step.
But Ms Young and others are demanding a complete overhaul of the police department, and say they will be back.
Mr Wright was pulled over for an expired tag on his car license plate. Family members and advocates say he was racially profiled.
Police released body camera footage on Monday showing Mr Wright fleeing from officers after they told him he was being arrested for an outstanding warrant.
As Mr Wright re-enters his car, Officer Potter is heard shouting "Taser" several times before firing a shot, apparently by mistake.
In a one-sentence resignation letter to city officials. Mrs Potter wrote that she "loved every minute of being a police officer... but I believe it is in the best interest of the community, the department, and my fellow officers if I resign immediately".
media captionPolice release footage of arrest and shooting of Daunte Wright.
Mr Wright's father, Aubrey Wright, told ABC News that he does not believe that Mrs Potter - a 26-year police veteran who trained other officers - mistook her gun for her Taser.
"I lost my son. He's never coming back. I can't accept that. A mistake? That doesn't even sound right. This officer has been on the force for 26 years. I can't accept that," he said.