On the eve of a legal battle in New York, Wayne LaPierre told board members on Friday that he would step down as the longtime chief of the National Rifle Association.

Mr. LaPierre, 74, has led the N.R.A., once one of the nation’s most prominent lobbying organizations, for more than three decades. But his resignation came as he faced his gravest challenge yet, a corruption trial in Manhattan amid a legal showdown with New York’s attorney general, Letitia James. Jury selection has already begun, and Mr. LaPierre has been in the courtroom for some of it. Opening arguments were scheduled for early next week.

Mr. LaPierre’s resignation, which is effective on Jan. 31, did not stem from a deal with the attorney general’s office, and Ms. James said on Friday that she expected the trial to go forward. Mr. LaPierre’s longtime spokesman, Andrew Arulanandam, will become the N.R.A.’s interim chief executive. The development was first reported by The Wall Street Journal.

“With pride in all that we have accomplished, I am announcing my resignation from the N.R.A.,” Mr. LaPierre said in a statement. “I’ve been a card-carrying member of this organization for most of my adult life, and I will never stop supporting the N.R.A. and its fight to defend Second Amendment freedom. My passion for our cause burns as deeply as ever.”

The announcement took place during a board meeting in Irving, Texas. The N.R.A. said Mr. LaPierre had attributed his decision to “health reasons.”

Since Ms. James began investigating the organization four years ago amid reports of runaway spending practices, the N.R.A. has said it has undertaken a reform effort. On Friday, the group reiterated that it was “committed to good governance” and said it had already “accepted reimbursement, with interest, for alleged excess benefit transactions from LaPierre.”

But Mr. LaPierre was seen as facing an uphill battle in trying to convince a New York judge to keep him in place, given what has already become public about his alleged mismanagement. Late last year, perhaps in anticipation of his departure, Mr. LaPierre elevated Mr. Arulanandam, a longtime loyalist.

Recently, speculation festered that there might be another bankruptcy filing on the eve of the trial. Instead, Mr. LaPierre announced his resignation, which will reshape the Manhattan case, since Ms. James was seeking to oust him.

She is still trying to bar Mr. LaPierre from holding any position at the group. She is also seeking financial penalties from him and three other defendants; those penalties would flow back to the N.R.A., which is a nonprofit group that was founded in New York and falls under Ms. James’s jurisdiction.

“The end of the Wayne LaPierre era at the N.R.A. is an important victory in our case,” Ms. James said in a social media post on Friday afternoon. “LaPierre’s resignation validates our claims against him, but it will not insulate him from accountability. We look forward to presenting our case in court.”

Mr. LaPierre played a leading role in transforming gun culture in America, but the last half decade of his tenure at the N.R.A. was marred by scandals and internal upheaval. In recent years, the group has been in a tailspin.

Membership has plummeted from nearly six million five years ago to 4.2 million today. Revenue is down 44 percent since 2016, according to internal audits, and legal costs have soared to tens of millions a year.

Nonetheless, the gun rights movement has become a bulwark of Republican politics during Mr. LaPierre’s years leading the N.R.A. A temporary assault weapons ban was signed into law early in his tenure; today, such measures are a nonstarter for Republicans, despite a proliferation of mass shootings.

Mr. LaPierre’s departure was the latest surprising turn in the N.R.A.’s strategy, which has been unpredictable since he turned in 2018 to a Texas lawyer, William A. Brewer III, to become the organization’s lead outside counsel. Mr. Brewer was the architect of a 2021 bankruptcy filing that was kept secret from the organization’s general counsel and most of its board. It was ultimately dismissed by a Texas judge.

Mr. Brewer, a Democrat, also recently enlisted the support of the American Civil Liberties Union in a federal lawsuit; that suit accuses former Gov. Andrew M. Cuomo and his administration of misusing their authority by dissuading banks and insurers from doing business with the N.R.A.

Mr. LaPierre’s testimony at the trial is likely to focus heavily on his spending practices. He was a regular for more than a decade at a Zegna boutique in Beverly Hills, where he spent nearly $40,000 in a single May 2004 outing, billing it through an N.R.A. contractor.

He also spent more than $250,000 on travel to, among other places, Palm Beach, Fla., Reno, Nev., the Bahamas and Lake Como in Italy. He has argued that these were legitimate business expenses.

As the corruption case has dragged on, Mr. LaPierre’s allies have dwindled, with some of his sharpest critics coming from within the N.R.A.

One of the other defendants in the case, Joshua Powell, has been in settlement talks with the attorney general’s office and a deal is seen as imminent.

Mr. Powell was the organization’s second-in-command for a time, but he later turned against Mr. LaPierre’s leadership and even called for some gun control measures, including universal background checks for those buying guns.

“This has been a long time coming and is far too late after governing over 30 years of corruption,” Mr. Powell said in an email. “At this point the N.R.A. is little more than a shell of itself after hemorrhaging hundreds of millions in legal fees. The N.R.A. will need a new strong dynamic leader to dig itself out of the deep hole it’s in.”

Gun control groups were happy to see Mr. LaPierre go.

“Thoughts and prayers,” said Nick Suplina, a former senior adviser and special counsel at the attorney general’s office who now works for the gun control advocacy group Everytown.

“I think the attorney general sought the removal of Wayne LaPierre as the head of the N.R.A. and she just got what she wanted,” he added.