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In April 2020, Frusciante announced that he would release a new solo album, entitled She Smiles Because She Presses the Button, under his Trickfinger alias in June 5, 2020.

Josh Klinghoffer on January 23, 2020, gave an interview with Marc Maron on his podcast WTF with Marc Maron where for the first time he discussed in detail his departure from the band. Klinghoffer said that the band met with him to inform him that John Frusciante would be returning to which he said he wasn't surprised because Frusciante had reached out to Anthony Kiedis shortly before that and that Flea and Frusciante had been jamming together for a while. Flea and Frusciante had such a connection with each other that he said he never truly had, even though Flea tried hard to connect with him musically as he did with Frusciante. When Frusciante quit the band in 2009, it put a bit of a strain on their friendship. Frusciante didn't seem very happy the band was continuing without him or with Klinghoffer and assumed they would break up. Klinghoffer said that he is happy though for Frusciante and that it is Frusciante's place to be in this band.

On December 15, 2019, The Red Hot Chili Peppers announced on their Instagram page that Josh Klinghoffer was leaving the band after 10 years and that Frusciante would take his place. The band's first three shows with Frusciante will be on May 15, 2020, at the Hangout Music Festival in Gulf Shores, AL, and May 22 at Napa Valley California's Bottlerock Festival and May 24 at the Boston Calling Music in Boston, MA. These shows will be followed by five festival dates outside the United States in June 2020. The band is currently in the process of writing their next album which they plan to release in 2020.

On June 13, 2017, Frusciante, under the alias of Trickfinger, announced that he would be releasing his second studio album Trickfinger II on September 8, 2017, on the label Acid Test. The six songs, which were never intended to be released, were originally recorded in 2007.

Acid Test Records announced on February 15, 2016, that Frusciante would release an EP of electronic music on April 16, 2016, entitled Foregrow. The EP was released on the 2016 Record Store Day and comprised the title track, recorded for RZA's film The Man with the Iron Fists, and three instrumental tracks.

In a 2015 interview, Cris Kirkwood said that following Frusciante's departure from the Chili Peppers in 1992, Frusciante auditioned for the Meat Puppets. Kirkwood said: "He showed up with his guitar out of its case and barefoot. We were on a major label then, we just got signed, and those guys had blown up to where they were at and John needed to get out. John gets to our pad and we started getting ready to play and I said, 'You want to use my tuner?' He said, 'No, I'll bend it in.' It was so far out. Then we jammed but it didn't come to anything. Maybe he wasn't in the right place and we were a tight little unit. It just didn't quite happen but it could have worked."

On November 24, 2015, Frusciante announced that he was releasing free unreleased songs dating from 2008 to 2013 on his official Bandcamp and SoundCloud pages. He also debunked the interview about him retiring from the music industry, saying that his words were taken out of context. The announcement was made via Frusciante's rarely updated website in an open letter titled "Hello audience," where Frusciante provides an in-depth response to the website that, according to him, took his words out of context. He writes, "I also must clear something up. I normally don't read my press, but I heard about this quote, recently taken out of context by some lame website and made into a headline, in which I said 'I have no audience'. This has been misinterpreted, and by no fault of the excellent journalist who interviewed me for the fine publication Electronic Beats. ... Obviously I have a public audience. I am aware of them, and they know who they are." He continues, "Reduced to a single sentence, it would have been accurate to say that, at this point, I have no particular audience in mind while I am making music."

In 2011, Frusciante married Nicole Turley, drummer and lead vocalist of the experimental band Swahili Blonde. On May 8, 2015, it was announced that Turley had filed for divorce. On October 3, 2015, Turley announced that she was seeking $75,000 a month as part of their divorce settlement. According to court documents, Turley, who was already being paid $20,000 a month, needed a higher payment to maintain her quality of living. She claimed her finances were down to $30,000. Turley said that Frusciante was worth $14 million and she was entitled to more money saying that together the couple employed a team of personal assistants, and owned three homes and a private music studio. A week later Frusciante responded to Turley's demands saying that he refuses to pay her any more money and that she is also seeking $2,600 a month for gifts and expenses for her adult brother. He also said he was done footing the bill for her musical career saying "I don't know if you can call her recording efforts a hobby or a pastime, ... but it seems improper to characterize Nicole as a professional musician." On October 19, 2015, a judge ruled in favor of Turley saying Frusciante had to pay his former wife $53,000 a month. Frusciante was also forced to pay $71,000 for Turley's legal expenses.

I don't need to take drugs. I feel so much more high all the time right now because of the type of momentum that a person can get going when you really dedicate yourself to something that you really love. I don't even consider doing them, they're completely silly. Between my dedication to trying to constantly be a better musician and eating my health foods and doing yoga, I feel so much more high than I did for the last few years of doing drugs. At this point I'm the happiest person in the world. These things do not fuck with me at all, and I'm so proud of that—you don't know how proud I am. It's such a beautiful thing to be able to face life, to face yourself, without hiding behind drugs; without having to have anger towards people who love you. There are people who are scared of losing stuff, but you don't lose anything for any other reason than if you just give up on yourself.

—John Frusciante (Rolling Stone, February 2007)

Frusciante's approach to album composition has changed. On his early recordings, he welcomed sonic imperfections, noting that "even on [To Record Only Water for Ten Days] there are off-pitch vocals and out-of-tune guitars." However, on later albums such as Shadows Collide With People, he pursued the opposite: "I just wanted everything to be perfect—I didn't want anything off pitch, or off time, or any unintentional this or that." Frusciante views songwriting as taking time, and does not force it: "If a song wants to come to me, I'm always ready to receive it, but I don't work at it." Much of his solo material is first written on an acoustic or unamplified electric guitar. He also prefers to record his albums on analog tapes and other relatively primitive equipment. This preference stems from his belief that older equipment can speed up the recording process, and that modern computerized recording technology gives only an illusion of efficiency. Frusciante tries to streamline the recording process as much as possible because he thinks "music comes alive when [you] are creating it fast". He also enjoys the challenge of having to record something in very few takes, and believes that when musicians are unable to handle the pressure of having to record something quickly they often get frustrated or bogged down by perfectionism. With his focus on new styles of music, Frusciante describes having worked with the computer as an instrument, and having found the ability to merge old and new production techniques. He has noted that there has been a change in how he works on an album. In the past, he would work on one song at a time, but with the new "Progressive Synth Pop" that he has been working on, he feels much more comfortable to work within the album as a whole. He currently uses the music tracker Renoise as his main Digital audio workstation along with some drum machines, sequencers, and other hardware, along with his Doepfer, Arp, and other modular synthesizers.

With his recent solo work, he has cited electronic music—in which the guitar is often completely absent—as an influence. His electronic music influences include Aphex Twin, Depeche Mode, New Order, The Human League, Ekkehard Ehlers, Peter Rehberg, and Christian Fennesz. His interests are constantly changing, as he believes that without change he will no longer have any interest in playing: "I'm always drawing inspiration from different kinds of music and playing guitar along with records, and I go into each new album project with a preconceived idea of what styles I want to combine."

Frusciante released an instrumental song named Wayne on April 7, 2013, through his website. It was written and dedicated to the memory of his late friend, former Red Hot Chili Peppers' tour chef Wayne Forman. Outsides, his fifth EP, was released on August 14, 2013 in Japan, and on August 27, 2013 worldwide. The same year, he began collaborating with Wu-Tang affiliates Black Knights (Crisis The Sharpshoota, The Rugged Monk). Medieval Chamber, the second album by Black Knights, was released on January 14, 2014. All the music featured on the record was produced by Frusciante, with a few tracks featuring his vocals as well. Frusciante also became involved in Kimono Kult, a project including his wife Nicole Turley, Omar Rodriguez-Lopez, Teri Gender Bender (Le Butcherettes, Bosnian Rainbows), string musician Laena Geronimo (Raw Geronimo) and guitarist Dante White (Dante Vs. Zombies, Starlite Desperation). Their debut EP, Hiding in the Light was produced by Turley and was released on her record label Neurotic Yell in March 2014. A track "Todo Menos El Dolor" was released on SoundCloud on January 16. Having released "Scratch", a single recorded during the PBX Funicular Intaglio Zone sessions, Frusciante released his eleventh studio album, Enclosure, on April 8, 2014. In April 2015, Frusciante released his first album under the alias of Trickfinger. The album of the same name is Frusciante's first experimenting with the acid house genre. He previously released an EP, Sect In Sgt under this alias in 2012.

Frusciante has received critical recognition for his guitar playing, ranking at number 18 on Rolling Stone' s list of "The 100 Greatest Guitarists of All Time" in 2003; and again in a second list published in 2011, where he ranked at number 72. He was ranked as number 42 in Gibson's list of the "50 Best Guitarists of All Time". He was voted "The Best Guitarist of the Last 30 Years" in a 2010 BBC poll called "The Axe Factor". Frusciante was inducted into the Rock and Roll Hall of Fame as a member of the Red Hot Chili Peppers on April 14, 2012, but did not attend the ceremony. In December 2019, Frusciante again joined the Red Hot Chili Peppers, resulting in the departure of Klinghoffer.

Frusciante released a new EP on July 17, 2012, entitled Letur-Lefr. As with his previous solo releases, it was released through Record Collection Music. Recorded in 2010, Letur-Lefr marked a clear departure from guitar-driven sound of Frusciante's previous albums and combined elements of abstract electronica, pop and hip hop. He followed the EP with his tenth full-length studio album PBX Funicular Intaglio Zone on September 25, 2012. Prior to that, on August 16, he also released a free download of the non-album song "Walls and Doors".

After his departure from the Red Hot Chili Peppers, Frusciante became more serious about his longtime dream to make electronic music. As he explained on his blog, "I started to learn how to program all the instruments we associate with Acid House music and some other hardware. Then I started recording, playing 10 or so synced machines through a small mixer into a CD burner. This was all experimental Acid House, my skills at making rock music playing no part in it whatsoever. I had lost interest in traditional songwriting and I was excited about finding new methods for creating music." During that time Frusciante began an electronic trio with Aaron Funk and Chris McDonald under the name Speed Dealer Moms. Their first EP was released in December 2010 on Planet Mu Records.

Frusciante continued to collaborate with his friend Omar Rodríguez-López. Along with providing guitar work to The Mars Volta's studio albums, The Bedlam in Goliath and Octahedron, and Rodríguez-López's solo albums Se Dice Bisonte, No Búfalo and Calibration (Is Pushing Luck and Key Too Far), he functioned as executive producer for Rodríguez-López's directorial film debut, The Sentimental Engine Slayer. The film debuted at the Rotterdam Film Festival in February 2010. Along with work on the film, Frusciante and Rodríguez-López have released two collaborative records in May 2010. The first is the album Omar Rodriguez-Lopez & John Frusciante, an album with just the two of them, the other a quartet record, Sepulcros de Miel, consisting of Rodríguez-López, Frusciante, Juan Alderete and Marcel Rodríguez-López.

Ataxia released its second and final studio album, AW II in 2007. Following the Stadium Arcadium tour (early May 2006 to late August 2007), the Red Hot Chili Peppers agreed to a hiatus of indefinite length. In early 2008, Anthony Kiedis finally confirmed this, citing exhaustion from constant work since Californication as the main reason. Frusciante quit the group on July 29, 2009, but did not publicly announce his departure until December 2009, two months after the band ended their hiatus in October 2009 and began work on their next album with Josh Klinghoffer as their new guitarist.

Frusciante's tenth solo album, The Empyrean, was released on January 20, 2009, through Record Collection. The record—a concept album—was in production between December 2006 and March 2008. The Empyrean features an array of musicians including Frusciante's Chili Peppers bandmate Flea, friends Josh Klinghoffer and former Smiths guitarist Johnny Marr, as well as guest musicians including Sonus Quartet and New Dimension Singers. Frusciante stated: "I'm really happy with [the record] and I've listened to it a lot for the psychedelic experience it provides," suggesting the album is "to be played as loud as possible and is suited to dark living rooms late at night."

Frusciante has stated that he became serious about creating and engineering his electronic music in 2007. As he progressed in enhancing his skills with electronic instruments and techniques, he has stated that he felt comfortable with how R&B and Hip hop music integrated into his work. He has noted that these and other new techniques were all influences on his EP, Letur-Lefr. PBX Funicular Intaglio Zone was recorded while Frusciante looked to find new ways to play the guitar with the new forms of music and production that he had been studying. In his blog post, "My Recent History," he notes that "Aspects of PBX are the realization of combinations of styles of music I saw in my head many years ago, as potentials, but which I had no idea how to execute."

During the recording of Blood Sugar Sex Magik, Captain Beefheart and the acoustic, one-man blues of Lead Belly and Robert Johnson, were among the most noteworthy influences. Frusciante cites R&B singer Brandy as a musical inspiration and admires her voice, calling it "multidimensional" and "inspiring." In describing her voice and signature sound, he said, "You can't hear [the elaborate harmonies] with your conscious; you have to hear her voice with your subconscious." He also mentioned that Brandy was the "main inspiration" behind the guitar work on Red Hot Chili Peppers' 2006 album, Stadium Arcadium.

In early 2005, Frusciante entered the studio to work on his fifth studio album with the Chili Peppers, Stadium Arcadium. His guitar playing is dominant throughout the album, and he provides backing vocals on most of the tracks. Although usually following a "less is more" style of guitar playing, he began using a full twenty-four track mixer for maximum effect. In the arrangements, he incorporates a wide array of sounds and playing styles, similar to the funk-influenced Blood Sugar Sex Magik or the more melodic By the Way. He also changed his approach to his playing, opting to contribute solos and let songs form from jam sessions. In an interview from Guitar World, Frusciante explained how he approached his guitar solos for their album Stadium Arcadium completely differently from those for their previous albums. On Blood Sugar Sex Magik and Californication, Frusciante had a general idea how he wanted his guitar solos to sound. For Stadium Arcadium, almost every guitar solo was completely improvised by Frusciante on the spot. Several reviews have stressed that the influence of Hendrix is evident in his solos on the album, with Frusciante himself backing this up. He also expanded the use of guitar effects throughout the album, and used various other instruments such as the synthesizer and mellotron. He worked continuously with Rubin over-dubbing guitar progressions, changing harmonies and using all his technical resources.

Frusciante began a series of collaborations with friend Omar Rodríguez-López and his band The Mars Volta, by contributing guitar and electronic instrumentation to song "Cicatriz ESP" off their album De-Loused in the Comatorium. He also contributed guitar solos on their 2005 album Frances the Mute. In 2006, he helped The Mars Volta complete their third album Amputechture by playing guitar on seven of its eight tracks. In return, Rodriguez-Lopez has played on several of Frusciante's solo albums, as well as making a guest appearance on Stadium Arcadium.

Frusciante wrote and recorded a plethora of songs during and after the By the Way tour. In February 2004, he started a side project with Joe Lally of Fugazi and Josh Klinghoffer, called Ataxia. The group was together for about two weeks, during which they recorded about ninety minutes of material. After two days in the recording studio, they played two shows at the Knitting Factory in Hollywood, and spent two more days in the studio before disbanding. Later that year, five songs provided by Frusciante appeared on The Brown Bunny soundtrack.

Frusciante released his fourth full-length solo album Shadows Collide with People on February 24, 2004. This featured guest appearances from some of his friends, including Klinghoffer, and Chili Peppers bandmates Smith and Flea. In June 2004, he announced that he would be releasing six records over six months: The Will to Death, Ataxia's Automatic Writing, DC EP, Inside of Emptiness, A Sphere in the Heart of Silence and Curtains. With the release of Curtains, Frusciante debuted his only music video of 2004, for the track "The Past Recedes". He wanted to produce these records quickly and inexpensively on analog tape, avoiding modern studio and computer-assisted recording processes. Frusciante noted, "These six records were recorded in a period of six months after coming home from touring with the Chili Peppers for one-and-a-half years. I made a list of all the songs I had and they totaled about seventy. My objective was to record as many songs as I could during the break that I had. In the midst of doing that, I was writing some of my best songs, so some of these albums have as many new songs as old songs. It was definitely the most productive time of my life."

Frusciante's musical style has evolved over the course of his career. Although he received moderate recognition for his early guitar work, it was not until later in his career that music critics and guitarists alike began to fully recognize it: in October 2003, he was ranked eighteenth in Rolling Stone's list of the "100 Greatest Guitarists of All Time". Frusciante attributes this recent recognition to his shift in focus, stating that he chose an approach based on rhythmic patterns inspired by the complexity of material Jimi Hendrix and Eddie Van Halen produced. On earlier records, however, much of his output was influenced by various underground punk and new wave musicians.

Frusciante has an active solo career, having released twelve solo albums and seven EPs; his recordings include elements ranging from experimental rock and ambient music to new wave and electronica. Frusciante also released two acid house albums and one EP under his alias Trickfinger. He has also recorded with numerous other artists, including the Mars Volta, for whom he was a studio guitarist (and occasional live performer) from 2002 until 2008; Josh Klinghoffer and Joe Lally, with whom he released two albums as Ataxia; and various collaborations with both Klinghoffer and Omar Rodríguez-López. He has also produced or recorded with Duran Duran, Wu-Tang Clan, Swahili Blonde, Black Knights, The Bicycle Thief, Glenn Hughes, Ziggy Marley, Johnny Cash, George Clinton, Johnny Marr, Dewa Budjana and others.

During the Californication world tour, Frusciante continued to compose new material, many of which would be released in 2001 on his third solo album To Record Only Water for Ten Days. The album was stylistically unlike his previous records, less markedly stream-of-consciousness or avant-garde. However, the lyrics were still very cryptic and its sound was notably stripped down. The songwriting and production of To Record Only Water for Ten Days were more efficient and straightforward than on his previous recordings. The album strayed from the alternative rock he had just written with the Chili Peppers on Californication, focusing more on electronic and new wave elements. In addition to his guitar work, Frusciante experimented with a variety of synthesizers, a distinctive feature of the record.

In 2001, Frusciante began recording his fourth album with Red Hot Chili Peppers, By the Way (2002); he considered the time to be among the happiest in his life. He relished the chance the album gave him to "keep writing better songs". While working on By the Way, he also composed most of what would become Shadows Collide with People, as well as the songs created for the movie The Brown Bunny. His goal to improve his guitar playing on the album was largely driven by a desire to emulate guitar players such as Johnny Marr, John McGeoch and Andy Partridge. He wanted to listen to these musicians "who weren't just about technique but more about textures", or as he put it, "people who used good chords". The album marked Frusciante's shift to a more group-minded mentality within the Chili Peppers, viewing the band as a cohesive unit rather than as four separate entities.

In early 1998, the Red Hot Chili Peppers fired guitarist Dave Navarro and were on the verge of breaking up. Flea told Kiedis, "the only way I could imagine carrying on [with the Red Hot Chili Peppers] is if we got John back in the band." With Frusciante free of his addictions and ailments, Kiedis and Flea thought it was an appropriate time to invite him back. When Flea visited him at his home and asked him to rejoin the band, Frusciante began sobbing and said: "nothing would make me happier in the world." With Frusciante back on guitar, the Chili Peppers began recording their next album, Californication, released in 1999. Frusciante's return restored a key component of the Chili Peppers' sound, as well as a healthy morale. He brought with him his deep devotion to music, which affected the band's recording style during the album. Frusciante has frequently stated that his work on Californication was his favorite.

With the Red Hot Chili Peppers, Frusciante provided backing vocals in a falsetto tenor, a style he started on Blood Sugar Sex Magik. He thoroughly enjoyed his role in the Chili Peppers as backing vocalist, and said that backing vocals are a "real art form". Despite his commitment to the Chili Peppers, he felt that his work with the band should remain separate from his solo projects. When he returned to the Chili Peppers in 1998, Kiedis wanted the band to record "Living in Hell", a song Frusciante had written several years before. Frusciante refused, feeling that the creative freedom he needed for his solo projects would have conflicted with his role in the band.

Frusciante released his second solo album, Smile from the Streets You Hold, in 1997. The album's first track, "Enter a Uh", is characterized by cryptic lyrics and hysterical screeches. Frusciante also coughs throughout the track, showcasing his deteriorating health. By his admission, he released the album to get "drug money" and withdrew it from the market in 1999. The album is also notable for including a recording called Height Down, which features River Phoenix.

In late 1996, after more than five years of addiction to heroin, Frusciante went cold turkey. However, months later he was still unable to break addictions to crack cocaine and alcohol. In January 1998, urged by his longtime friend Bob Forrest, Frusciante checked into Las Encinas, a drug rehabilitation clinic in Pasadena. He was diagnosed with a potentially lethal oral infection, which could only be alleviated by removing his rotten teeth and replacing them with dental implants. He also received skin grafts to help repair the abscesses on his ravaged arms. About a month later, Frusciante checked out of Las Encinas and re-entered society.

Frusciante released his first solo album, Niandra Lades and Usually Just a T-Shirt, on March 8, 1994. Frusciante denied that it was recorded while he was on heroin, saying it was released when he was a heroin addict. The album is an avant-garde composition whose initial purpose was a spiritual and emotional expression: "I wrote [the record] because I was in a really big place in my head—it was a huge, spiritual place telling me what to do. As long as I'm obeying those forces, it's always going to be meaningful. I could be playing guitar and I could say 'Play something that sucks,' and if I'm in that place, it's gonna be great. And it has nothing to do with me, except in ways that can't be understood." Niandra Lades and Usually Just a T-Shirt was released on Rick Rubin's label American Recordings. Warner Bros., the Chili Peppers' label, owned rights to the album because of the leaving-artist clause in Frusciante's Chili Peppers contract. However, because he was reclusive, the label handed the rights over to Rubin, who released the album at the urging of Frusciante's friends.

According to Bob Forrest in his 2013 memoir Running With Monsters, actor River Phoenix, a friend of Frusciante and the Chili Peppers, was living with Frusciante in late October 1993. Forrest said that the two would do large amounts of drugs together, embarking on binges and barely sleeping. On the evening of October 30, 1993, Phoenix was to perform with the band P—which featured Flea, actor Johnny Depp, Gibby Haynes of the Butthole Surfers, and Al Jourgensen of Ministry—at The Viper Room, a Hollywood nightclub partly owned at the time by Depp. Forrest claims that Phoenix and Frusciante arrived at the club to meet Phoenix's girlfriend Samantha Mathis, Phoenix's brother Joaquin, and their sister Rain. In the early morning hours of October 31, Phoenix was found outside on the sidewalk overdosing, suffering from convulsions. He was rushed by ambulance to the hospital (with Flea riding with him) and was pronounced dead shortly after. Frusciante has never commented on Phoenix's death and it is unknown where Frusciante was at the time of Phoenix's death.

Frusciante also began to feel that destiny was leading him away from the band. When the Chili Peppers began their world tour, he started to hear voices in his head telling him "you won't make it during the tour, you have to go now." Frusciante admitted to having once taken great pleasure in hedonism; however, "by the age of 20, I started doing it right and looking at it as an artistic expression instead of a way of partying and screwing a bunch of girls. To balance it out, I had to be extra-humble, extra-anti-rock star." He refused to take the stage during a performance at Tokyo's Club Quattro on May 7, 1992, telling his bandmates that he was leaving the band. He was persuaded to perform but left for California the next morning. "It was just impossible for me to stay in the band any longer," he said. "It had come to the point where even though they wanted me in the band, it felt like I was forced out of the band. Not by any members in particular or management in particular, but just the direction it was going." He was replaced by former Jane's Addiction guitarist Dave Navarro.

Frusciante developed serious drug habits while touring with the band during the previous four years. He said that when he "found out that Flea was stoned out of his mind at every show, that inspired me to be a pothead". Frusciante was smoking large amounts of marijuana and began to use heroin and was on the verge of full-scale addiction. Upon returning to California in 1992, Frusciante entered a deep depression, feeling that his life was over and that he could no longer write music or play the guitar. He focused on painting, producing 4-track recordings he had made while working on Blood Sugar Sex Magik, and writing short stories and screenplays. To cope with his worsening depression, Frusciante increased his heroin use and spiraled into a life-threatening dependency. His use of heroin to medicate his depression was a clear decision: "I was very sad, and I was always happy when I was on drugs; therefore, I should be on drugs all the time. I was never guilty—I was always really proud to be an addict."

The Chili Peppers collaborated with producer Rick Rubin for their second record with Frusciante, Blood Sugar Sex Magik (1991). Rubin felt that it was important to record the album in an unorthodox setting, and suggested an old Hollywood Hills mansion. Frusciante, Kiedis and Flea isolated themselves there for the duration of the recording. Frusciante and Flea seldom went outside, and spent most of their time smoking marijuana. Around this time, Frusciante began a side project with Flea and Jane's Addiction drummer Stephen Perkins, the Three Amoebas. They recorded roughly ten to fifteen hours of material, which went unreleased.

At the age of eighteen, he joined the Red Hot Chili Peppers, first appearing on the band's 1989 album, Mother's Milk. The group's follow-up album, Blood Sugar Sex Magik (1991), was a breakthrough success. Frusciante became overwhelmed by the band's new popularity and quit in 1992. He became a recluse and entered a long period of drug addiction, during which he released his first solo recordings: Niandra Lades and Usually Just a T-Shirt (1994) and Smile from the Streets You Hold (1997). In 1998, he completed drug rehabilitation and rejoined the Red Hot Chili Peppers. Their next album, Californication (1999), would eventually go on to sell 15.4 million copies. His album To Record Only Water for Ten Days was released in 2001. A fourth album with the Chili Peppers, By the Way, was released in 2002. On a creative spree, Frusciante released six solo albums in 2004; each album explored different recording techniques and genres. 2006 saw the release of his fifth album with the Chili Peppers, Stadium Arcadium. In 2009, Frusciante released The Empyrean, which features Flea and Josh Klinghoffer, and announced he had again parted ways with the Chili Peppers.

Frusciante was not familiar with the funk genre of Red Hot Chili Peppers' sound: "I wasn't really a funk player before I joined the band. I learned everything I needed to know about how to sound good with Flea by studying Hillel's playing and I just took it sideways from there." Several weeks into the band's new lineup, Peligro, whose performance was suffering due to extreme drug abuse, was fired. Soon after, Chad Smith was recruited as drummer and the new lineup began recording their first album, Mother's Milk (1989). Frusciante focused on emulating Slovak's style. Producer Michael Beinhorn disagreed, and wanted Frusciante to play with an uncharacteristic heavy metal tone, largely absent from the band's three preceding records. Frusciante and Beinhorn fought frequently over guitar tone and layering; Beinhorn prevailed as Frusciante felt pressured by his knowledge of the studio. Kiedis recalls that "[Beinhorn] wanted John to have a big, crunching, almost metal-sounding guitar tone whereas before we always had some interesting acid-rock guitar tones as well as a lot of slinky, sexy, funky guitar tones."

Frusciante became friends with former Dead Kennedys drummer D. H. Peligro in early 1988. They jammed together, and Peligro invited his friend, Chili Peppers bassist Flea. Frusciante and Flea developed musical chemistry immediately, with Flea later acknowledging that might have been the day he first played the bass riff to the future Chili Peppers track "Nobody Weird Like Me". Around the same time, Frusciante intended to audition for Frank Zappa's band, but changed his mind as Zappa strictly prohibited illegal drug use. Frusciante said, "I realized that I wanted to be a rock star, do drugs and get girls, and that I wouldn't be able to do that if I was in Zappa's band."

Slovak died of a heroin overdose in 1988. Red Hot Chili Peppers drummer Jack Irons, devastated, left the group. Remaining members Flea and vocalist Anthony Kiedis recruited Peligro on drums and DeWayne "Blackbyrd" McKnight, formerly of P-Funk, on guitar. McKnight, however, failed to connect musically within the group. Flea proposed auditioning Frusciante, whose intimate knowledge of the Chili Peppers' repertoire impressed him. Flea and Kiedis auditioned him and agreed that he would be a suitable replacement for McKnight. When Flea called Frusciante with the news of his acceptance into the Chili Peppers, Frusciante ran through his house screaming with joy, and jumped on a wall, leaving permanent boot marks. He was considering a contract with Thelonious Monster at the time—and had been playing with the act for two weeks—but his unanticipated reception into the Chili Peppers prompted him to change his plans.

Frusciante's first major influence was Jimi Hendrix. He then saw The Red Hot Chili Peppers (at that point, The was part of their name) in concert in 1985, after which their then-guitarist Hillel Slovak became his second major influence, with Frusciante coming to idolize Slovak. Although Hendrix and Slovak were arguably Frusciante's most profound influences, he was also inspired by glam rock artists David Bowie, and T. Rex; as well as avant-garde acts such as Syd Barrett, Captain Beefheart, The Residents, The Velvet Underground, Neu!, Frank Zappa, and Kraftwerk. Frusciante seems to be much influenced by the progressive rock acts like Genesis, King Crimson, Van der Graaf Generator, and Yes mentioning them in multiple interviews. Frusciante wrote an essay for the Yes The Word Is Live box set, released in 2005.

Frusciante discovered the Red Hot Chili Peppers around 1984 when his guitar instructor was auditioning as a guitarist for them. Frusciante attended a Red Hot Chili Peppers performance at the age of fifteen and rapidly became a devoted fan. He idolized guitarist Hillel Slovak, familiarizing himself with virtually all the guitar and bass parts from the Chili Peppers' first three records. He became acquainted with Slovak; the two spoke months before Slovak's death:

John Anthony Frusciante (/f r uː ˈ ʃ ɑː n t eɪ / ( listen ) ; born March 5, 1970) is an American musician, singer, songwriter, and producer best known as the lead guitarist of the rock band Red Hot Chili Peppers across three stints (1988–1992, 1998–2009, 2019–present). He has recorded five studio albums with them.

Frusciante was born in Queens, New York, on March 5, 1970. Frusciante is of Italian descent; his paternal great-grandfather Generoso Frusciante emigrated from Benevento. His father, John Sr., is a Juilliard-trained pianist, and his mother Gail was a promising vocalist who gave up her career to be a stay-at-home mother. Frusciante's family moved to Tucson, Arizona, and then Florida, where his father served as a Broward County judge until October 2010. His parents separated, and he and his mother moved to Santa Monica, California.

In general, his sound is also defined by an affinity for vintage guitars. All the guitars that he owns, records, and tours with were made before 1970. Frusciante uses the specific guitar that he finds appropriate for a certain song. All of the guitars he owned before quitting the band were destroyed when his house burned down in 1996. The first guitar he bought after rejoining the Chili Peppers was a 1962 red Fender Jaguar. His most-often used guitar, however, is a 1962 Sunburst Fender Stratocaster that was given to him as a gift from Anthony Kiedis after Frusciante rejoined the Chili Peppers in 1998. He has played this guitar on every album since rejoining the Chili Peppers, and their ensuing tours. He also owns a 1955 Fender Stratocaster, his only Strat with a maple neck. Frusciante's most highly appraised instrument is a 1955 Gretsch White Falcon, which he used twice per show during the By the Way tour. He has since stopped using it, saying there was "no room for it". Virtually all of Frusciante's acoustic work is played with a 1950s Martin 0–15.

Frusciante's guitar playing employs emphasis on appropriate melody, tone, and structure rather than virtuosity. Although virtuoso influences can be heard throughout his career, he has said that he often minimizes this. He feels that in general, guitar mastery has not evolved much since the 1960s and considers the greatest players of that decade unsurpassed. When he was growing up in the 1980s, many mainstream guitarists focused on speed. Because of this, he thinks that the skills of many defiant new wave and punk guitarists were largely overlooked. Therefore, he accentuates the melodically driven technique of players such as Matthew Ashman of Bow Wow Wow and Bernard Sumner of Joy Division as much as possible because he thinks that their style has been overlooked and consequently underexplored. Despite this, he considers himself a fan of technique-driven guitarists like Randy Rhoads and Steve Vai, but represses an urge to emulate their style: "People believe that by playing faster and creating new playing techniques you can progress forward, but then they realize that emotionally they don't progress at all. They transmit nothing to the people listening and they stay at where Hendrix was three decades ago. Something like that happened to Vai in the 80s." Believing that focusing only on "clean tones" is negative, Frusciante developed an interest in playing with what he calls a "grimy" sound. As a result, he considers it beneficial to "mistreat" his guitar and employ various forms of distortion when soloing. He also tries to break as many "stylistic boundaries" as he can to expand his musical horizons. He thinks that much of the output from today's guitarists is unoriginal and that many of his contemporaries "follow the rules with no risk".