The defendants have all been picked up and held in detention since the start of the conflict eight years ago, which has left at least 20,000 dead in the country's remote northeast.
To date, just 13 people have been put on trial and only nine convicted for their links to the Islamist insurgency, according to official figures.
The most high-profile current case is that of Khalid Al- Barnawi, a leader of the Boko Haram offshoot Ansaru, who is charged with the abduction and murder of 10 foreign nationals.
Some 1,670 detainees at a military base in Kainji, in the central state of Niger, will be tried first followed by 651 others held at the Giwa barracks in the capital of the northeastern state of Borno state, Maiduguri.
More From This Section
"It's the first significant trial of Boko Haram suspects," said Matthew Page, a former US State Department analyst and a specialist on Nigeria.
But he told AFP that while "positive" it was still a "very small step", as many of the detainees had been held in custody for years, without access to a lawyer or ever having appeared before a judge.
A justice ministry source said no media would be allowed on security grounds and that although civilian courts, they would be held in military facilities.
Umar Ado, a defence lawyer based in Nigeria's biggest northern city, Kano, said that was "as good as denying the public the right to know how the trial is carried out".
"It sends the wrong signal that justice is not served or the process is compromised," he added.
There have also been questions about the ability of Nigeria's justice system to handle so many cases at once and even of simple procedural details such as whether defendants will be tried on their own or together.
To what extent those on trial are connected to the group will likely come under scrutiny.
"There are good reasons to believe that large numbers of the detainees have very little or no connection at all to the group," said Matthew Page.
Amnesty International said in a damning June 2015 report that more than 20,000 people had been arbitrarily arrested as part of the fight against Boko Haram.
It highlighted appalling conditions at military detention facilities and claimed at least 1,200 people had been summarily killed and 7,000 died in custody since 2011.