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The dean of students and a school counselor are accused of making a bad situation worse in a meeting with the gunman and his parents just hours before the mass shooting.
James Crumbley joins his wife, who was convicted in February on identical charges.
Both the prosecution and defense rested early Wednesday morning.
As during his wife's trial last month, Crumbley's defense team implied Oxford High School staff members were responsible for the mass shooting that occurred there in 2021.
James is the last of the three-member Crumbley family to face trial for their role in the worst school shooting in Michigan history. His wife awaits sentencing in April, and his son will spend the rest of his life behind bars.
James Crumbley's wife was found guilty in February on the same manslaughter charges he now faces.
The Oxford, Michigan, school shooter's father faces trial on identical charges next month.
The jury will begin deliberations next week on if Jennifer Crumbley can be held responsible for her son's crimes.
Jennifer Crumbley said she wishes her son would have killed her and her husband instead of four schoolmates.
The owner of a coffee company said police had "full-on rifles" while arresting Jennifer and James Crumbley.
One witness said she was more worried about her job than what her son had done.
The presiding judge dismissed jurors for the day shortly after Crumbley's lawyer called one witness' testimony prejudicial.
Prosecutors painted Jennifer Crumbley as more worried about her horse than her son's mental health.
Attorneys made opening statements in the trial of Jennifer Crumbley, who along with her husband are the first parents to face criminal charges related to a school shooting.
Victims of the Oxford High School shooting confronted the shooter at the sentencing hearing where they called him a coward and detailed the personal traumas they would deal with for the rest of their lives.
The investigative firm commissioned by Oxford school officials found that there were protocols in place to deal with troubled students, but a lack of trained workers at all levels allowed the tragedy to unfold despite warning signs.
The couple have been in jail for almost two years as they contest the involuntary manslaughter charges against them. They now likely face trial, unless they can cut a deal with prosecutors.
While the defense argued that the shooter, who was 15 at the time of his crimes, was too young to face life in prison, the prosecution was adamantly against the idea of parole. Sentencing is scheduled for Dec. 8.
At a hearing that will determine if the shooter gets a life prison sentence, defense lawyers painted him as a severely depressed youth with a closed head injury and detached parents who refused to acknowledge his mental deterioration.
“I just watched him kill someone,” one student texted his family in a group chat as he hid in a bathroom.