The 47-year-old history and geography teacher was stabbed and then beheaded near his secondary school in the Paris suburb of Conflans-Sainte-Honorine.
His attacker, 18-year-old Chechen refugee Abdoullakh Anzorov, was shot dead at the scene by police.
The young radicalised Islamist murdered Paty after messages spread on social media that the teacher had shown his class cartoons of the Prophet Mohammed from the satirical magazine Charlie Hebdo.
Paty had used the magazine as part of an ethics class to discuss free speech laws in France, where blasphemy is legal and cartoons mocking religious figures have a long history.
His killing took place just weeks after Charlie Hebdo republished the cartoons. When the magazine first used the images in 2015, Islamic gunmen stormed its office, killing 12 people.
Last month another teacher, Dominique Bernard, was killed in Arras in northern France by a young radicalised Islamist.
Five of the adolescents on trial, who were 14 or 15 at the time of Paty's murder, will be judged behind closed doors in juvenile court for criminal conspiracy with intent to cause violence.
They are accused of having been on the lookout for Paty and identifying him to the killer in exchange for money.
Spiral of events
A sixth teenager, who was 13 at the time, is accused of false accusation for wrongly saying that Paty had asked Muslim students to identify themselves and leave the classroom before he showed the cartoons.
In fact, the schoolgirl had not attended Paty's class that day.
Her false allegation sparked violent outbursts on social media by her father, Brahim Chnina, and militant Islamist Abdelhakim Sefrioui, who made several videos denouncing Paty by name.
The two men will be judged in a criminal court in late 2024 along with six other adults.
Paty's family see the trial of the teenagers as crucial, according to Virginie Le Roy, a lawyer representing his parents and one of his sisters.
"The role of the minors was fundamental in the sequence of events that led to his assassination," she said.
The prosecutors' case traces events over 10 days leading up to the murder, from the schoolgirl lie to online attacks and the killer's arrival at the school on October 16.
According to the enquiry, Anzarov approaches a teenager outside the school and says: "Hey kid. Comme and see. I've something to propose to you."
He offers the boy 300 euros ($300) to identify Paty, saying he wants to film the teacher "saying sorry".
The boy "boasts" to other teenagers about the offer, not wanting to do it alone. Four others join him.'There he is'
They go back and forth between the school and Anzorov's hiding place, act as lookouts or film themselves with the money.
Anzorov asks one of the boys to ring the girl at the source of the stories about Paty.
She repeats the lie.
The girl later told investigators she did not know Anzorov was listening to the conversation.
When Paty leaves the school, the boys tell Anzorov: "There he is."
The teacher is murdered just before 5:00 pm.
During questioning, when they broke down in tears, the teenagers swore that at most they thought Paty would be "flagged up on social media", "humiliated" or maybe "roughed up" but they never imagined "it would go as far as murder".
They now are high school students and risk two-and-a-half years in prison.
"It is complicated," said Dylan Slama, the lawyer for one of the accused.
"He will be associated with this for the rest of his life."
The trial is scheduled to last until December 8.
