Johnathan Blake was born in Philadelphia on July 1, 1976, the son of the jazz violinist John Blake Jr., who played with Grover Washington Jr. in the late 1970s and with McCoy Tyner in the early 1980s before leading six albums of his own for Gramavision and Sunnyside. Blake has always named his father as his chief mentor, and his first exposure to live music came from watching him work. He was started on violin at three. By his own account in his SmallsLIVE biography, he took a music aptitude test at ten, scored perfectly, and switched to drums, which is where he stayed. His early training came through the Settlement Music School and the Lovett Hines Youth Ensemble, the Philadelphia program that also produced the alto saxophonist Jaleel Shaw, whom Blake met there and has recorded with ever since. At George Washington High School he was drum captain of the marching band.

He went on to jazz studies at William Paterson University, where his teachers were the bassist Rufus Reid, the drummers John Riley and Horacee Arnold, and the saxophonist Steve Wilson, and he was working professionally before he graduated. The first bandleaders to hire him were Oliver Lake, whose big band he joined, then Roy Hargrove and David Sanchez. His earliest surviving recording credit is the pianist Norman Simmons' The Heat And The Sweet (Milljac MJP 1007), assembled from sessions in March 1996, December 1996, and May 1997, with Rufus Reid on bass. In 2006 he won an ASCAP Young Jazz Composers Award, and in 2007 he completed a master's degree in composition at Rutgers University, where he studied with Victor Lewis, Ralph Bowen, Conrad Herwig, and Stanley Cowell.

The band that made his name in New York was the Mingus Big Band. He first recorded with it on Blues & Politics (Dreyfus, 1999), produced by Sue Mingus, and he shared the drum chair on the two Grammy-nominated albums that followed: Tonight at Noon... Three or Four Shades of Love (Dreyfus, from December 2001 and November 2001 sessions at Avatar Studios), where he is credited on drums and tambourine alongside Jeff "Tain" Watts, and I Am Three (Sue Mingus Music, from October and November 2004 sessions in Brooklyn and New Jersey). Working nightly inside Charles Mingus' book, in a section that changed every week, is where he learned to hold a large ensemble together. He was still with the band twenty-three years later, on The Charles Mingus Centennial Sessions (Candid, 2022) and its second volume in 2024.

His long apprenticeship as a first-call sideman ran the whole of the 2000s. He recorded with the trumpeter Alex Sipiagin at Systems Two in June 2002, with the pianist Rob Schneiderman and the bassist Boris Kozlov on the co-billed trio date Back In Town (Reservoir, recorded January 22, 2004), with Russell Malone's trio live at the Jazz Standard in September 2005, and with Jaleel Shaw on both of his early leader albums. In July 2006 the Israeli bassist Omer Avital took a sextet into Systems Two in Brooklyn for two days and cut Arrival (Fresh Sound Records FSWJ 035), with Blake on drums, tambourine, and vocals beside Jason Lindner, Joel Frahm, Avi Lebovich, and the trumpeter Avishai E. Cohen. The same band minus the trombone came back four years later for the Avital quintet's Live At Smalls (SmallsLIVE SL0014, 2010), taped at the club in Greenwich Village. Two months before the Arrival session Blake had also cut Makin' It with the Oliver Lake Organ Trio, the record that put his name on the cover alongside Lake and the organist Jared Gold.

The chair that defined the decade was Tom Harrell's. Blake joined the trumpeter's quintet with Wayne Escoffery, Danny Grissett, and Ugonna Okegwo for Light On (HighNote HCD 7171), recorded at the Rudy Van Gelder studio in Englewood Cliffs on December 5 and 7, 2006 with Van Gelder himself engineering, and stayed for nine albums across twelve years: Prana Dance (2009), Roman Nights (2010), The Time of the Sun (2011), the equally billed Number Five (2012), Colors of a Dream (2013) with Esperanza Spalding on bass and voice, First Impressions (2015), Something Gold Something Blue (2016), which brought Omer Avital back onto one of his records playing oud, and finally Infinity (HighNote HCD 7321), cut at Sear Sound on September 24 and 30, 2018 with Mark Turner in the tenor chair. The other long association began at Avatar Studios on July 3 and 4, 2015, when he recorded Book of Intuition with Kenny Barron and Kiyoshi Kitagawa, a Grammy-nominated trio record. Blake has held the drum chair in Barron's working trio ever since, through Concentric Circles (Blue Note, from March 2017), the co-billed Without Deception with Dave Holland (Dare2, 2020), Beyond This Place (Artwork, from February 2023), and Songbook (Artwork, 2025). Blue Note's own artist copy describes the tenure as "nearly 15 years," which places its start well before the first record.

He came late to leading. The Eleventh Hour (Sunnyside SSC 1304) appeared in 2012, when he was 35, with Jaleel Shaw, Mark Turner, Kevin Hays, and Ben Street, and guest turns from Robert Glasper, Tom Harrell, Tim Warfield, and the harmonica player Gregoire Maret. Gone, But Not Forgotten (Criss Cross Jazz 1368) followed on February 20, 2014, a piano-less two-tenor quartet with Chris Potter, Turner, and Street, cut in a single day at RPM Studios in Astoria. In January 2018 he took a trio with Potter and the bassist Linda May Han Oh into The Jazz Gallery for two nights and released the results as the double album Trion on Jimmy Katz's non-profit label Giant Step Arts. In the same period he co-founded the Black Art Jazz Collective, the cooperative sextet with Wayne Escoffery, Jeremy Pelt, James Burton III, Xavier Davis, and Vicente Archer, which has made three albums since 2016.

Blake signed to Blue Note and released Homeward Bound on October 29, 2021, introducing Pentad, a quintet with Immanuel Wilkins on alto saxophone, Joel Ross on vibraphone, David Virelles on piano, and Dezron Douglas on bass. He built the band, he has said, for a fuller and more chordal sound than the trios and quartets he had been leading, and named it for five individuals coming together for a common cause. Its title track is written for Ana Grace Marquez-Greene, the daughter of the saxophonist Jimmy Greene, a longtime friend, who was killed in the Sandy Hook Elementary School shooting in December 2012. The same quintet made Passage (Blue Note, August 2023), an homage to his father, who had passed away on August 15, 2014; its ten tracks include pieces by Douglas, Virelles, John Blake Jr., and the drummer Ralph Peterson, and the cover photograph is by Eugene Wood, Blake's godfather. His third Blue Note album, My Life Matters, arrived on September 19, 2025: a fourteen-part suite commissioned by The Jazz Gallery, written as a treatise on family and on the obligation to stand up against injustice, with Dayna Stephens, Fabian Almazan, Jalen Baker, and Douglas, guest appearances from the vocalist Bilal and the turntablist DJ Jahi Sundance, and both of his children on the record, his son Johna on electric bass and his daughter Muna as a reader. Alongside the leader dates he has kept an unusually wide sideman book: three albums with Dr. Lonnie Smith for Blue Note, Bill Frisell's quartet record Four (Blue Note, 2022), the Maria Schneider Orchestra's Data Lords (ArtistShare, from sessions at Oktaven Audio in late summer 2019), two ECM albums with Oded Tzur, and the Kris Davis Trio's Run The Gauntlet (Pyroclastic, from January 2024), on which he also carries a composer credit.

Blake is a swing drummer first, and everything else follows from that. NPR Music has called him "the ultimate modernist," but the quality his employers keep describing is an older one: Chris Potter has said of him that "the depth of his jazz swing feeling" is such that "he feels it and he lives it with his entire self," and singled out his ride cymbal. He works from pocket and narrative rather than display, and what makes him a first call across such different bands is that he rebuilds his approach for each one: broad and greasy behind Dr. Lonnie Smith's Hammond B3, propulsive and conversational with Kenny Barron, coloristic and almost weightless on Oded Tzur's ECM records, and a section anchor inside the Mingus Big Band and the Maria Schneider Orchestra. He inherited a specific city's drumming lineage: SFJazz's profile of him places him in the Philadelphia line that runs through Philly Joe Jones, Mickey Roker, Joe Chambers, Sunny Murray, and Donald Bailey. His father's example matters as much as any drummer's: it was John Blake Jr. who taught him to hear a tune as a melody before hearing it as a groove, which is audible in the writing on Passage and in the long-form architecture of My Life Matters. As a composer he has an ASCAP Young Jazz Composers Award (2006), a commission and fellowship from The Jazz Gallery with a residency at the Pocantico Center in Tarrytown (2017), and a habit of returning to his own pieces across records: "West Berkley St." appears both on Trion in 2018 and on Passage five years later.