Born in Bridgeport, Connecticut on October 16, 1977, Mayer grew up in nearby Fairfield, the second of three sons. There, he became friends with future tennis star James Blake. Mayer attended Fairfield High School (now Fairfield Warde High School) for most of high school, although he attended Brien McMahon High School in Norwalk, Connecticut for his junior year, where he was enrolled in the Center for Global Studies at Brien McMahon High School. Then known as the Center for Japanese Studies Abroad, it is a magnet program for students in Fairfield County wanting to learn Japanese.

Mayer listened to pop music, but it was not until the age of thirteen that his aspiration for playing the guitar was realized, and his father rented one for him. On Late Night with Conan O'Brien, Mayer confessed that he had played the clarinet for a while in grammar school, with minor success.

Generally, it was believed that Mayer's father, a Bridgeport High School principal, had given him a confiscated tape player that contained an album by Stevie Ray Vaughan. However, Mayer, in a 2006 interview on the New Zealand show Close Up said the cassette was given to him by a neighbor, sparking Mayer's love of the blues. After two years of practice, he started playing at blues bars and other venues in the area. While in high school, he was in a band called Villanova Junction with Joe Beleznay, Tim Procaccini, and Rich Wolf.

When Mayer was seventeen, he was suddenly stricken with a cardiac arrhythmia that sent him to the hospital for a weekend. The trauma of the incident sparked his songwriting, and he penned his first lyrics the night he got home. Shortly thereafter, he began suffering from crippling panic attacks and even now he keeps Xanax (an anti-anxiety drug) with him, just in case.

After playing the guitar for several years, Mayer enrolled in the Berklee College of Music in Boston, Massachusetts, at the age of nineteen. After two semesters, he chose to cut his studies short in favor of a move to Atlanta, Georgia, with his college friend and band mate, Clay Cook. As a Georgia native, it was Cook's idea to move to Atlanta, and as fate would have it, his coercion of Mayer was right, as the two began their career in earnest there, quickly making a name for the two-man band, LoFi Masters. They frequented the local coffee house and club circuit in venues like Eddie's Attic. Cook cites that the two were expressing musical differences, as Mayer wanted to take the duo to more of a pop direction, which was not where he had wanted to take it. The two parted ways and Mayer the began his solo career.

With the help of local producer and engineer Glenn Matullo, Mayer recorded the independent EP Inside Wants Out. Cook is also cited as the co-writer of many of the songs from the EP, most notably, Mayer's first commercial single release "No Such Thing." The EP includes only eight songs, all with Mayer on vocals and guitars and on the first track "Back To You", a full band was enlisted, including the EP's co-producer David "De-La" LaBruyere on bass guitars. Mayer and LaBruyere then began to tour locally throughout Georgia and the surrounding states.

Mayer's name began to grow and was brought to the attention of "launch" label Aware Records. After some time of having his songs included on the Aware Compilations, continuous songwriting and touring in the Aware Festival concerts, in early 2001, he released an internet-only album entitled Room for Squares through Aware. During that time, Aware inked a deal with Columbia Records which gave Columbia first option to sign Aware artists, and thus, in September of the same year, Columbia remixed and re-released Room for Squares (artwork was also updated, as well as adding 3x5, which didn't appear on the original). This "debut" included the first half of the songs that had been previously released on his independent release.

By the end of 2002, Room for Squares had spawned several radio hits, including "No Such Thing," "Your Body Is a Wonderland," and, ultimately, "Why Georgia" as a radio-only single. In 2003, he won a Grammy for Best Male Pop Vocal Performance for the 2002 release of "Your Body Is a Wonderland." In his acceptance speech, he remarked, "This is very, very fast, and I promise to catch up." In Mayer's acceptance speech, he ambigiously mentioned "being 16" in his speech. This was mistaken by many to suggest he was only 16 years old at the time. Mayer has since clarified that he meant that compared to his contemporaries, he felt very young to be winning such an accolade.

In 2003, Mayer released a live CD and DVD of a concert in Birmingham, Alabama entitled Any Given Thursday which went on to moderate success, related to other albums, but respectable success as compared to other live albums. The concert features songs previously not heard, such as "Man on the Side", a song he'd written with Clay Cook, "Covered In Rain" which according to a documentary included in the DVD release, is the "part two" to Room for Squares's song "City Love" (in which a line in the bridge is "Covered In Rain"). The concert also features the song "Something's Missing" which later appeared on Mayer's followup album Heavier Things and as of 2007, is the only song to have appeared on every live release Mayer has contributed to.

In 2003, Mayer released the follow-up album, Heavier Things. This album also brought critical and commercial success. Although the album did top the charts for a time, it ultimately did not sell as well as Room for Squares. However, Mayer's most successful single to date, "Daughters," yielded Mayer a Grammy for Song of the Year in 2005. For this award, he beat contenders Alicia Keys and Kanye West. He dedicated the award to his grandmother, Annie Hoffman, who passed away in May 2004. He also won Best Male Pop Vocal Performance, beating Elvis Costello, Prince, and Seal for the award. Mayer also was honored with the Hal David Starlight Award (previously the Starlight Award) at the 37th Annual Songwriters Hall of Fame Induction Ceremony in 2006.

In 2004, as the followup to his second studio album, Mayer again had live concerts recorded, but this time the recordings were across several nights of his U.S. tour. These recordings were released under the title as/is, indicating that there was no post production in the recordings, so all the errors were included as well as the good moments. According to Mayer, this "kept him honest". The recordings were across seven nights from the tour. Four of these nights were released for sale to the iTunes music store and a few months later, a CD was compiled with the "best of" the as/is nights, but also with the addition of an extra song not released in the first four releases: a cover of Marvin Gaye's song Inner City Blues (Make Me Wanna Holler) featuring a solo from Mayer's support act, Jazz and Blues Turntablist DJ Logic. All of the covers of the as/is releases featured drawings of bunnies in situations uncharacteristic for bunnies, such as at the laundromat or forming a wave.

In 2004, Mayer worked with hip hop artist and producer Kanye West, appearing both on rapper Common's song "Go!" and being included initially on West's album Late Registration, though their collaboration "Bittersweet" remains unreleased. Due to these collaborations, Mayer has received praise from rap heavyweights like Jay-Z and Nelly. When asked about his presence in the hip hop community, he said that, "It's not music out there right now. That's why, to me, hip-hop is where rock used to be."

It was around this time that Mayer began hinting a change in his musical interests, announcing that he was "closing up shop on acoustic sensitivity." In 2005, he began a string of collaborations with various important and provocative blues artists, including Buddy Guy, B.B. King, Eric Clapton, and jazz artist John Scofield. He also toured with legendary jazz pianist Herbie Hancock, which included a show at the Bonnaroo Music Festival in Manchester, Tennessee. These collaborations led to recordings with several of these artists, namely, Clapton (Back Home, Crossroads Guitar Festival), Guy (Bring 'Em In), Scofield (That's What I Say) and King (80).

Although Mayer has maintained a reputation for being a sensitive, meticulous singer-songwriter, he has also gained distinction as an accomplished guitarist, influenced by the likes of the above artists, as well as Jimi Hendrix, Stevie Ray Vaughan, and Freddie King.

In the spring of 2005, Mayer formed the John Mayer Trio with bassist Pino Palladino and drummer Steve Jordan, both of whom he had met through previous studio sessions. The trio played a combination of blues and rock music. In October 2005, the Trio opened for The Rolling Stones during a sold-out club tour of their own. In November 2005, they released a live album called Try! The first single, "Who Did You Think I Was?," lyrically underscores Mayer's decision to move away from acoustic pop music, especially indicating blues as his intended direction with the line "Got a brand new blues that I can't explain".

The John Mayer Trio took a break in mid-2006. John declared at the end of their performance at the Tempe Music Festival in March of 2006, "This is Steve Jordan, that's Pino Palladino, and I'm John Mayer. And for a few more minutes, we are the John Mayer Trio." On September 12, however, he announced plans for the Trio to begin work on a studio album, though specific details have yet to be provided.

Mayer's latest album, entitled Continuum, was released on September 12, 2006, and was produced by Mayer himself and John Mayer Trio drummer Steve Jordan. Mayer suggested the album was intended to combine his signature pop music with the feel, sound, groove and sensibilities of the blues. In that vein, two of the tracks from his trio release Try! — the funky "Vultures" and the blues centrepiece "Gravity" — also were included on Continuum.

The first single from Continuum was "Waiting on the World to Change," which debuted on The Ron and Fez Show. The song was the third most downloaded song of the week on the iTunes Music Store following its release on July 11, 2006, and debuted at #25 on the Billboard Hot 100 Chart. On August 23, 2006, Mayer debuted the entire album on the Los Angeles radio station Star 98.7, giving commentary on each and every track. A subsequent version was released the next day on the Clear Channel Music website as a streaming sneak preview. On September 22, 2006, Mayer appeared on CSI, playing live (albeit abridged) versions of "Waiting on the World to Change" and another track from Continuum, "Slow Dancing in a Burning Room." The song "Gravity" was featured on the television series House in the episode "Cane & Able".

On December 7, 2006, the 2007 Grammy nominees were announced. Mayer was nominated for five Grammys including the prestigious Album of the Year. John Mayer Trio also received a nomination for their album Try!. He won two: Best Pop Song with Vocal for "Waiting on the World to Change" and Best Pop Album for Continuum.

In a December blog entry Mayer announced he had begun writing new material. He has also indicated that he's in the studio experimenting with music in a sort of a blend of jazz (mentioning Elvin Jones as inspiration) and pop — aiming to produce what he calls today's "modern music," as jazz was once called.

Mayer remixed an acoustic version of his single, "Waiting on the World to Change" with vocal additions from fellow musician Ben Harper. In preparation for recording Continuum, Mayer booked the Village Recorder in Los Angeles to record five demo acoustic versions of his songs with veteran musician Robbie McIntosh. This was released on December 12, 2006 as an EP entitled The Village Sessions. As usual, Mayer oversaw the artwork of the release.

Mayer made the cover of Rolling Stone (#1020) in February 2007, along with John Frusciante and Derek Trucks. He was named as one of the "New Guitar Gods" and the cover nicknamed him "Slowhand, Jr.," a reference to Eric Clapton.

In 2003, Martin Guitars gave Mayer his own signature model acoustic guitar called the OM-28 John Mayer. The guitar was limited to a run of only 404, Atlanta's area code. This acoustic was followed by the release of a signature Stratocaster electric guitar by Fender guitars in 2005 — three different models in total. Unlike the Martin, two of Mayer's Signature Fender Stratocasters are not limited edition models, and can be found at many Fender dealers. The third Stratocaster, finished in charcoal frost metallic paint with racing stripe, was limited to only 100 guitars. In August 2006, Fender started manufacturing SERIES II John Mayer stratocasters. The new Olympic white with mint green pickguard and cream plastics replaced the shoreline gold model. Mayer is a passionate collector of guitars, and (as of 2006) his collection was estimated at over 200.

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