In 2008 Tillman joined the band Fleet Foxes as their drummer during the tour for their first record; he went on to play on their second album, Helplessness Blues (2011).

The album was a radical departure from his previous output, featuring a more marked, indie rock sound and satirical lyrics.

Honeybear was followed by another concept album, Pure Comedy (2017), exchanging the romantic content of the former for a nihilistic view of society, consumerism, and politics.

[9][10] As a record producer and songwriter, Tillman has also made contributions to albums by more mainstream artists such as Beyoncé,[11] Lady Gaga,[12] Kid Cudi,[13] Lana Del Rey, and Post Malone.

In 2006, the independent label Fargo Records released Tillman's first properly distributed solo album, Minor Works, and reissued I Will Return and Long May You Run as a two-disc set the same year.

[25] After signing to independent record label Western Vinyl, Tillman released two albums in 2009, Vacilando Territory Blues and Year in the Kingdom.

[23] Tillman said he wrote the title track of Vacilando Territory Blues to describe imagery he associates with his move to Seattle.

[21] After extensive touring with Fleet Foxes, promoting their album Helplessness Blues, Tillman played his final show with the band in Tokyo on January 20, 2012.

Dissatisfied with the slow and sad music he had previously made, he adopted the performing name of Father John Misty.

[30] Tillman wrote an essay about Damien Jurado's recording, Brothers and Sisters of the Eternal Son (Secretly Canadian, 2014).

[31] He also wrote the soundtrack for a short film called The History of Caves, directed by his wife, filmmaker Emma Elizabeth Tillman.

The poster text further states that the release will be sold as "compact disc" as well as "[l]imited edition prismatic hologram 6xLP on merlot and emerald semi-translucent 180 gram vinyl with original alternate-side etchings by Josh Tillman available till[sic] supplies last".

Tillman gained media attention on July 22, 2016, after walking off stage at XPoNential Music Festival in Camden, New Jersey, after twenty minutes into his planned fifty-minute performance.

"[41] He finally played a thirteen-minute piece from his then-upcoming album Pure Comedy called "Leaving LA" which references the frustrations he spoke of during his speech.

Tillman then covered Leonard Cohen's "Bird on the Wire" before telling the crowd he loved them and walked off the stage, cutting his performance short.

[43] In September 2016, his voice and likeness were featured in Brad Neely's animated surreal comedy show Harg Nallin' Sclopio Peepio on Adult Swim.

The song features an animated Father John Misty singing what appears to be a humorous parody of his music, with lyrics most likely written by Brad Neely.

The lyrics describe how Americans "die doing the dumbest of crap," such as riding unicycles, ghost hunting, and performing stunts while cosplaying as Batman.

[46] On January 23, 2017, the title track from Misty's third studio album, Pure Comedy, was released with an accompanying music video.

[55] The album was announced on April 18 and was released on June 1; its track listing was shared, alongside two further songs, "Disappointing Diamonds Are The Rarest Of Them All" and "Just Dumb Enough to Try".

"[57] Tillman also contributed to the soundtrack of Hotel Artemis with the song "Gilded Cage", which was released on June 8, 2018, the same day as the film.

[61] It was announced Father John Misty's fifth studio album, Chloë and the Next 20th Century, would be released on April 8, 2022, by Sub Pop and Bella Union.

On September 17, Tillman released the album's second single, "Screamland", which features Low's Alan Sparhawk on guitar.

[77] Tillman met photographer Emma Elizabeth Garr after he moved to the Laurel Canyon neighborhood of Los Angeles in 2011.