Headley, 52, a U.S. citizen of Pakistani descent, admitted he attended training camps in Pakistan operated by the terrorist group Lashkar-e-Toiba on five occasions from 2002 to 2005, and traveled to India five times to conduct surveillance before the Mumbai massacre.
He faced possible life in the prison after pleading guilty to 12 counts for his role in planning the November 2008 Mumbai attack, which killed at least 160 people, including six Americans, and an aborted attack on a Danish newspaper over the printing of a cartoon of the Prophet Muhammad.
In handing down the 35-year sentence Thursday U.S. District Judge Harry Leinenweber said he wanted to make sure Headley is "never in a position to commit a terrorist attack."
Although Headley cooperated with authorities investigating the Mumbai attack, Leinenweber said he should be "under lock and key for the rest of his life.
"Mr. Headley is a terrorist," the judge said.
"There is little question that life imprisonment would be an appropriate punishment for Headley's incredibly serious crimes but for the significant value provided by his immediate and extensive cooperation," prosecutors said in seeking a lesser sentence of 30 to 35 years.
Former U.S. Attorney Patrick Fitzgerald said at the hearing Headley had "freely admitted" his role in the Mumbai attack when he was arrested at O'Hare International Airport and asked the judge to consider Headley's cooperation in imposing his sentence, the Chicago Tribune reported.
Seven people, including Headley's childhood friend from Pakistan, Tahawwur Rana, were charged with terrorism. Rana was sentenced to 14 years last week in the Denmark plot.