The brothers are currently serving life in prison without the possibility of parole in California.
The Los Angeles County district attorney formally recommended their resentencing in a court filing on Friday, arguing for a lesser sentence for the pair. If approved, the request would make the brothers eligible for parole.
While it is a significant development in a case that has gripped the nation, it is one step on what could be a long road.
And not everyone is happy at the prospect of them potentially regaining their freedom.
Resentencing request includes details from time in prison
The 57-page court motion filed by the district attorney's office, obtained by BBC News, includes a timeline of the case, an argument for why the Menendez brothers should be resentenced and details of their time behind bars.
The filing includes glowing recommendations from prison officials and various programmes the brothers launched behind bars that aimed to help other inmates, including those who were victims of childhood trauma and disabled or elderly inmates. It also includes the educational degrees both brothers received while serving their sentences.
All of this was done, the report notes, "without any expectation or hope of ever being released".
It also includes the 30-year discipline records for both Erik Menendez and Lyle Menendez. Both brothers were cited for possessing a mobile phone in a cell they shared with other inmates.
Erik Menendez had several other violations, including two fights, in 2011 and 1997.
It notes that Lyle Menendez was never cited for any fights and had to be moved from the general population to the "special needs" area of the prison in 1997 because "he wouldn't fight back when attacked". He was cited twice for contraband - a lighter in 2013 and a new pair of Adidas sneakers in 1998 that a "female visitor brought him".
"While incarcerated, Erik and Lyle Menendez have transformed and taken advantage of meaningful opportunities to mature, move beyond criminal thinking, repent, and become a productive community members," the filing states, adding they are "ready to reenter society".
What happens next?
Friday's filing provides the basis for the district attorney office's argument that will be made before a judge on why the brothers should be resentenced.
The next step is to schedule a resentencing hearing, where a judge will hear arguments for and against the change.
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The office of George Gascón, the Los Angeles County district attorney, is asking they be sentenced for murder.
Under Californian law - based on the age they were at the time of the crimes - that would make them "eligible for parole immediately," the district attorney said at a news conference Thursday.
His office says they hope to schedule the hearing sometime in the next 30-45 days and say it is possible Lyle and Erik Menendez may attend the proceeding.
The hearing is likely to be contentious. Mr Gascón noted that this case has divided his office and members of his staff might argue against him in court.
If the hearing results in a judge approving the new sentence, attention will shift to the California parole board.
The board will examine the case and whether the Menendez brothers are a threat to society if they are released.
Even if the board approves their release, Governor Gavin Newsom could decide to halt proceedings.
What has the Menendez family been saying?
Earlier this month, more than two dozen members of the Menendez family issued a public plea for Erik and Lyle to be released 35 years after killing their parents, Jose and Kitty Menendez.
Those family members alleged the boys endured horrific sexual abuse at the hands of their father and are not a threat to society.
Kitty Menendez's sister, Joan Anderson VanderMolen, argued “the whole world wasn’t ready to believe that the boys could be raped, or that young men could be victims of sexual violence".
She said that now “we know better" and "a jury today would never deliver such a harsh sentence".
But the family isn't in total agreement.
A lawyer for Kitty Menendez’s brother, Milton Andersen, called the brothers "cold-blooded" and said their "actions shattered their family and left a trail of grief that has persisted for decades."
"Jose was shot six times, and Kitty was shot ten times, including a shot to her face after Erik reloaded."
Mr Andersen believes his nephews should stay in prison for their "heinous act", according to his lawyer, Kathy Cady.
Why is this happening - 35 years after the killings?
Neama Rahmani, a criminal defence attorney and former federal prosecutor, told the BBC that a "perfect storm of PR and politics" has led to the Menendez brothers having a real shot at freedom.
He noted the recent attention the case has gotten from celebrities, a Netflix drama and docuseries on the case, and an "embattled" district attorney vying to remain in office.
"You're never going to see another case like this. It's a unicorn."
The Menendez brothers filed a motion in May 2023 detailing new evidence in their case and requesting their convictions be vacated.
Mr Gascón said his office had been reviewing the case for more than a year, but he said he made the decision to recommend their resentencing Thursday, only an hour before holding a highly publicised news conference on the landmark case.
The decision was announced 12 days before election day, in which Mr Gascón is running for re-election as Los Angeles county district attorney and is down by 30 points in some polls. He has denied his announcement was political and said it was a long-time coming.
The decision also came amid renewed attention in the case spurred by a new Netflix drama, Monsters: The Lyle and Erik Menendez Story as well as the release of docudrama, The Menendez Brothers.
The series introduced the case to a new generation and garnered attention from celebrities - including Kim Kardashian and Rosie O'Donnell - who called for the brothers to be released.
Why did the Menendez brothers kill their parents?
Motive has long been at the heart of this case.
Prosecutors painted the brothers as spoiled rich kids, who killed their wealthy parents in their Beverly Hills mansion so they could access their $14m (£10.7m) fortune.
They argued the duo methodically bought shotguns and fatally shot their parents a total of 13 times as the couple watched TV. They then went gambling, to parties and on shopping sprees, buying things like Rolex watches.
It was ultimately a confession to a psychologist that helped lead to their arrest when the girlfriend of their doctor audiotaped their admission and reported it to authorities.
The brothers ultimately admitted to the killings - but argued they acted out of self-defence after years of emotional, physical and sexual abuse.
They told the court they feared their parents would kill them if they didn’t act first. Lyle and Erik testified they confronted their parents about the sexual abuse and things had become combative in their household and they believed their parents were planning to kill them.
Family members testified about the abuse they witnessed - but none said they saw sexual abuse first-hand.
The twists and turns in the story made it infamous and even 35 years later it continues to be the catalyst for new documentaries and films.