WASHINGTON—Paul Manafort pleaded guilty to two federal crimes and agreed to cooperate with prosecutors, a dramatic turnaround for the former Trump campaign chairman who now becomes a powerful asset for special counsel Robert Mueller’s investigation.

Mr. Manafort, who has long struck a defiant posture toward Mr. Mueller, becomes the fifth associate of President Trump’s to plead guilty in connection with the special counsel’s probe, which is examining, among other things, any potential coordination between Moscow and Trump campaign officials in 2016.

None of Mr. Manafort’s crimes that he admitted Friday—or was convicted of in a separate trial in Virginia last month—relate to such coordination. But his cooperation agreement is far-reaching, requiring him to be “fully debriefed,” provide relevant materials, “participate in undercover activities” and testify whenever requested by Mr. Mueller’s office.

Mr. Manafort could help prosecutors as they piece together information about Russia and whether Mr. Trump obstructed justice by firing Federal Bureau of Investigation Director James Comey in May 2017. For one thing, Mr. Manafort is the first person to cooperate with Mr. Mueller who also attended a June 2016 meeting at Trump Tower that has drawn the special counsel’s interest. That session included Mr. Manafort; Donald Trump Jr.; Mr. Trump’s son-in-law Jared Kushner; and several Russians who had promised incriminating information about Democrat Hillary Clinton.

Related Video A jury found Paul Manafort, President Trump’s former campaign manager, guilty of eight counts of fraud, but couldn't reach a verdict on 10 other counts. Photo: Associated Press

Mr. Trump has denied any wrongdoing, and in a brief telephone interview Friday said that the Manafort case had nothing to do with him. “I got hit with an artificial witch hunt that should never have happened,” Mr. Trump said.

Still, that the former campaign chairman is now cooperating with the special counsel is likely to heighten the legal and political pressure on Mr. Trump, less than two months before midterm elections.

Mr. Manafort, appearing in court in a dark suit Friday, admitted to conspiring against the U.S. and obstructing justice.

“I plead guilty,” he said softly as he faced the judge, after one of Mr. Mueller’s prosecutors gave a lengthy recitation of Mr. Manafort’s misdeeds that included leading an effort for years that lobbied Washington officials on behalf of the Ukraine government without reporting it.

Mr. Manafort, 69 years old, had been convicted last month by a federal jury in Virginia of not reporting to tax authorities more than $16 million he earned between 2010 to 2014 for political consulting work in Ukraine, and he faced eight to 10 years in prison based on that conviction. He has been in jail since June after being accused of trying to influence the testimony of a potential witness.

He would have risked more prison time with a second criminal trial that was to start Monday on charges of conspiring against the U.S., conspiring to launder money, failing to register foreign lobbying work, misleading the government and obstruction of justice.

Mr. Manafort now faces as much as 10 additional years based on his plea. But prosecutors agreed to request a lesser sentence if Mr. Manafort provides them with substantial assistance.

After Friday’s court hearing, Manafort attorney Kevin Downing told reporters Mr. Manafort “accepted responsibility” and “wanted to make sure his family was able to remain safe and live a good life.” Mr. Downing had previously said Mr. Manafort would not cooperate with Mr. Mueller.

Mr. Manafort’s longstanding resistance to federal prosecutors, even while other figures pleaded guilty, had drawn praise from Mr. Trump, who called his previous trial “sad” and at one point lauded Mr. Manafort for having “refused to ‘break’ - make up stories in order to get a ‘deal.’ ” In a Fox News interview last month, Mr. Trump decried the longstanding prosecutorial practice of offering defendants leniency in exchange for information.

It isn’t clear what effect Mr. Manafort’s cooperation will have on the chances that Mr. Trump will pardon his former campaign chairman, which Democrats and some Republicans have warned would set off a political firestorm.

Trump lawyer Rudy Giuliani said in a text message Friday that Mr. Manafort’s decision to cooperate did not affect the possibility of a pardon. Asked if Mr. Trump might still do so, Mr. Giuliani said, “No comment, but I don’t know of anything preventing it.”

Mr. Manafort now joins former Trump national security adviser Mike Flynn and others in cooperating with Mr. Mueller. Three other longtime Trump confidants, including his former personal lawyer, Michael Cohen, have provided information to prosecutors in New York in a campaign-finance investigation that has implicated the president.

Mr. Manafort, in connection with Friday’s agreement, agreed to forfeit some of his multimillion-dollar homes, including a Brooklyn townhome and an estate on Long Island, as well as funds in multiple bank accounts.

Mr. Manafort’s trial in Virginia, which concluded in August, involved days of detailed testimony from people who had worked with and for Mr. Manafort. The testimony included embarrassing accounts of Mr. Manafort’s spending habits and what appeared to be deliberate efforts to mislead banks, accountants and his own bookkeeper about his income and expenses.

He was found guilty on eight counts, and the jury deadlocked on 10 others. Mr. Manafort admitted guilt on those 10 charges as part of Friday’s agreement.

The cases against Mr. Manafort are not related to the special counsel’s core mission of investigating Russia’s actions related to the 2016 election. Rather, they have focused on his work for former Ukrainian President Viktor Yanukovych, who was ousted and fled to Russia in 2014. That work was performed in the decade before Mr. Manafort served as Mr. Trump’s campaign chairman for several months in 2016.

As part of the plea, Mr. Manafort said the Ukraine work included shaping U.S. perception of Mr. Yanukovych and his pro-Russia party. He admitted he didn’t register as a foreign agent until June 2017, after he had misled federal investigators about the nature of his efforts.

He helped pay a law firm $4 million for its work on a report used to bolster Ukraine’s prosecution of Mr. Yanukovych’s political rival, Yulia Tymoshenko. But he used offshore accounts to pay the firm so Ukraine could falsely assert the report cost $12,000, according to the court document.

In court documents associated with the guilty plea, Mr. Manafort acknowledged that part of his work on behalf of Mr. Yanukovych included “an all out campaign to try to kill” congressional efforts to scrutinize him.

In May 2013, the document said, Mr. Manafort asked lobbyists “to write and disseminate within the United States news stories that alleged that” Ms. Tymoshenko “had paid for the murder of a Ukrainian official.” He directed the lobbyists to leave “no fingerprints.”

Mr. Manafort also used charges of anti-Semitism to try to tarnish the image of Ms. Tymoshenko, and then turn Jewish sentiment against the Obama administration in the U.S., the court document says.

He spread stories, for example, that an Obama cabinet member who had criticized Mr. Yanukovych “was supporting anti-Semitism because the official supported Tymoshenko, who in turn had formed a political alliance with a Ukraine party that espoused anti-Semitic views,” the court papers said.

He planted that idea with the media, according to the document. “I have someone pushing it on the NY Post. Bada bing bada boom,” he told a colleague, referring to the New York newspaper, the document said.

—Andrew Duehren, Rebecca Ballhaus and Peter Nicholas contributed to this article.

Write to Aruna Viswanatha at Aruna.Viswanatha@wsj.com