Manning, a 25-year-old former intelligence analyst from Oklahoma, has admitted to giving troves of information to the anti-secrecy website WikiLeaks, but military prosecutors are trying to prove Manning aided the enemy, which carries a potential life sentence.
"This is a case of about what happens when arrogance meets access to sensitive information," Capt. Joe Morrow said in his opening statement.
Manning's supporters hail him as a whistleblowing hero and political prisoner. Others say he is a traitor who endangered lives and national security.
"This, your honor, this is a case about a soldier who systematically harvested hundreds of thousands of documents from classified databases and then dumped that information on to the Internet into the hands of the enemy," Morrow said.
Manning's defense will give its opening statement later Monday. Manning has said he did not believe the information would harm the U.S. and he wanted to start a debate on the role of the military and foreign policy.
Manning, a slightly built soldier, sat calmly in the courtroom in his dark green dress uniform as the trial began.
He chose to have his court-martial heard by a judge instead of a jury. It is expected to run all summer.
More than three years ago, Manning was arrested in Iraq. Since then, he admitted to sending the material to the anti-secrecy website WikiLeaks and pleaded guilty to charges that would send him to prison for up to 20 years. The U.S. military and the Obama administration weren't satisfied, though, and pursued a charge of aiding the enemy, among others.
It's the most high-profile case for an administration that has come under criticism for its crackdown on leakers. The six prosecutions since Obama took office is more than in all other presidencies combined.
In February, Manning told military judge Army Col. Denise Lind he leaked the material to expose the American military's "bloodlust" and disregard for human life in Iraq and Afghanistan.
The judge accepted his guilty plea to reduced charges for about half of the alleged offenses, but prosecutors did not did not and moved forward with a court-martial on charges that also include violations of the Espionage Act and the Computer Fraud and Abuse Act.
U.S. officials have said the more than 700,000 Iraq and Afghanistan battlefield reports and State Department cables sent to WikiLeaks endangered lives and national security.
The material WikiLeaks began publishing in 2010 documented complaints of Iraqi detainee abuses; a U.S. tally of civilian deaths in Iraq; and America's weak support for the government of Tunisia — a disclosure Manning supporters said encouraged the popular uprising that ousted the Tunisian president in 2011 and helped trigger the Middle Eastern pro-democracy uprisings known as the Arab Spring.
Last month, the government agreed to accept Manning's guilty plea for a lesser version of one count, involving a single diplomatic cable summarizing U.S. embassy discussions with Icelandic officials about the country's financial troubles.
Manning also acknowledged sending WikiLeaks unclassified video of a 2007 U.S. Apache helicopter attack that killed civilians, including a Reuters photographer. An internal military investigation concluded the troops reasonably mistook the camera equipment for weapons; WikiLeaks dubbed the video "Collateral Murder."
The release of the cables and video embarrassed the U.S. and its allies. The Obama administration has said it threatened valuable military and diplomatic sources and strained America's relations with other governments, but the specific amount of damage hasn't been publicly revealed and probably won't be during the trial.
Lind ruled the extent of any damage is irrelevant. Defense attorney David Coombs contends it was minimal.
Much of the evidence is classified, which means large portions of the trial are likely to be closed to reporters and the public.
Lead prosecutor Maj. Ashden Fein told Lind in February that more than half of the government's 141 anticipated witnesses would testify about classified information, which would close up to 30 percent of the trial.
The court-martial's high degree of secrecy, including refusals to promptly release even routine filings and rulings, has fueled protests by Manning supporters. The Bradley Manning Support Network says it has raised more than $1.1 million for his defense and public outreach.
Supporters include documentary filmmaker Michael Moore, musician Graham Nash, actor John Cusack and Pentagon Papers leaker Daniel Ellsberg.
Ellsberg, a former military analyst, has said Manning's disclosures may be more significant than his own leak of a top-secret history of the Vietnam War expansion in 1971.
About 20 Manning supporters demonstrated in the rain outside the visitor gate at Fort Meade. They waved signs reading "free Bradley Manning" and "protect the truth" while chanting "What do want? Free Bradley. When do we want it? Now."
Manning's case gained even more attention when human rights groups and the United Nations' chief torture investigator complained about his pretrial confinement at a Marine Corps brig in Quantico, Va.
For nine months, Manning was held alone in a windowless cell 23 hours a day, sometimes with no clothing. Brig officials said it was to keep him from hurting himself or others.
Lind ruled Manning had been illegally punished and should get 112 days off any prison sentence he receives. Manning was moved in April 2011 to less restrictive conditions at Fort Leavenworth, Kansas.
Manning has said he corresponded online with someone he believed to be WikiLeaks founder Julian Assange but never confirmed the person's identity. Assange is the subject of a separate federal investigation into whether he can be prosecuted for publishing the information Manning leaked.
WikiLeaks has been careful never to confirm or deny Manning was the source of the documents.
Assange has been holed up in the Ecuadorean Embassy in London to avoid extradition to Sweden on sex-crimes allegations.