Hallie Biden, a former girlfriend of Hunter Biden and widow of his brother, Beau, took the stand on Thursday, telling jurors that she saw him buy, stash and smoke vast amounts of crack cocaine in the fall of 2018 when he claimed to be drug-free on a firearms application.

Ms. Biden — speaking in nervous, clipped bursts as she faced Mr. Biden across the fourth-floor courtroom — admitted that he had introduced her to crack in the summer of 2018. She said she was ashamed and embarrassed by their behavior when the two briefly lived together in a rented house in Annapolis, Md., a time when both were in shock over Beau Biden’s death.

“It was a terrible experience that I went through,” she said.

Ms. Biden is, by far, the most important witness for the prosecution, offering the most detailed, and intimate, portrait of Mr. Biden’s reckless and self-destructive behavior at the time.

Mr. Biden, she said, bought multiple rocks of crack in Washington, where he kept an apartment — some the size of “Ping-Pong balls, or bigger maybe” — and stored them in his “backpack or car.”

Ms. Biden said she discovered the gun at the center of the case when she was rifling through Mr. Biden’s vehicle the morning after he showed up at her house. It was part of a “pattern” of erratic behavior, she added, saying he would be unreachable for weeks at a time and she or her children would scrounge through his car for drugs or alcohol to help him “start anew and deal with stuff” when he reappeared exhausted at her home.

When she searched the car on Oct. 23, she described noticing “a dusting of powder” that she assumed to be “remnants of crack cocaine” before finding the gun in a case with a broken lock. Flustered, she said she improvised a way to dispose of it at a grocery store nearby.

Prosecutors then showed surveillance video of her tossing the gun only to return later and frantically try to recover it. “I realize it was a stupid idea now, but I was just so panicked” she said.

Earlier, Mr. Biden’s defense team suggested that it would try to challenge Ms. Biden’s credibility on cross-examination by introducing new text messages — some “salacious” — showing that she was enraged at him over his infidelity and drug abuse.

David C. Weiss, the special counsel who has brought a separate case against Mr. Biden involving more serious tax offenses, has turned to the women closest to Mr. Biden to document his drug use, revisiting some of the most damaging episodes in the Biden family’s recent history as the campaign season intensifies.

Ms. Biden, who was closest to Mr. Biden when he bought the gun, is likely to offer the most complete accounting of actions laid out in his indictment over his claim to be drug-free on a federal firearms form.

On Wednesday, two of Mr. Biden’s former romantic partners, his ex-wife and an ex-girlfriend, provided vivid and gut-wrenching testimony about his addiction to crack in the weeks and months before he applied for a gun.

Almost all the events at issue in the trial happened in 2018, when Joseph R. Biden Jr. was out of office.

A lawyer for Hunter Biden, Abbe Lowell, has suggested he could seek to undercut Ms. Biden’s narrative. In his opening statement on Tuesday, he drew a sharp distinction in the handling of the gun. During the 11 days that Mr. Biden owned the firearm, he never loaded it, never removed it from its lock box in his truck and never used it, Mr. Lowell said. It was his girlfriend at the time, Ms. Biden, who found the gun, removed it from the box, placed it in a pouch that contained drug residue and tossed it in a trash can.

Mr. Biden is charged with three felonies: lying to a federally licensed gun dealer, making a false claim on the federal firearms application and possessing an illegally obtained gun in October 2018. If convicted, Mr. Biden could face up to 25 years in prison and $750,000 in fines. But nonviolent first-time offenders who have not been accused of using the weapon in another crime rarely receive serious prison time for the charges.

The government’s case turns on a relatively straightforward question: whether Mr. Biden was abusing drugs when he filled out the federal firearms application claiming he was not an “unlawful user” of controlled substances. “Addiction may not be a choice, but lying and buying a gun is a choice,” Derek Hines, a top deputy to Mr. Weiss, told jurors in opening statements on Tuesday.

The sheer amount of unflattering evidence assembled by Mr. Weiss is intended to prove that Mr. Biden knowingly lied when he claimed not to be taking drugs when he bought the handgun. But it has, in the view of even some Biden family critics, moved far beyond that goal — into a publicly humiliating trial of the president’s troubled son for an offense that, while a crime, is seldom prosecuted as a stand-alone charge for someone with no prior criminal record who has been sober for years.