A six-week trial in Birmingham was told Benjamin Monk fired a Taser three times -- including a single 33-second discharge -- and left two bootlace prints on Atkinson's forehead during the incident on August 15, 2016.
Jurors took nearly 19 hours to reach unanimous verdicts on Monk, whom prosecutors said had exaggerated the threat posed by the former Aston Villa player and lied about the events to justify excessive and unlawful force.
The trial was told the 48-year-old star went into cardiac arrest after being taken from the scene, near his father's home in Telford, about 30 miles (48 kilometres) from Birmingham, in an ambulance, and was pronounced dead in hospital about an hour after he was tasered.
Monk, who was cleared of an alternative charge of murder, maintained his actions were lawful self-defence.
The 43-year-old officer was granted bail until sentencing at the same court on Monday. He was told by the judge that "a custodial sentence in his case is inevitable".
Jurors are still deliberating over an assault charge relating to Monk's colleague and former girlfriend, police constable Mary Ellen Bettley-Smith.
Following the verdict, charity INQUEST said no British police officer had been found guilty of murder or manslaughter following a death in custody or after police contact in England and Wales since 1986.
Director Deborah Coles said the "historic" verdict sent a strong message that officers were not above the law.
"Dalian's death is not an isolated case but part of a systemic problem," she said.
"For decades black men, particularly those in mental health crisis, have disproportionately died following use of force by police.
"True justice requires structural change across our society and its institutions to address racism, and respond better to mental ill-health and state violence."
Atkinson's family said the former footballer, a high-profile forward for Aston Villa in the early 1990s, who also played for Sheffield Wednesday, Ipswich and Real Sociedad, was "much missed".
"We are hugely relieved that the whole country now knows the truth about how Dalian died," said a family statement.
"While it has been hard for us not to be able to talk about the details of Dalian's death, it has been even harder to sit through this trial and to hear PC Monk try to justify the force he used."