[14][15] Romita was working at the New York City company Forbes Lithograph in 1949, earning $30 a week, when comic book inker Lester Zakarin,[16] a friend from high school whom he ran into on a subway train, offered him either $17[17] or $20[14] a page to pencil a 10-page story, possibly a crime comic about 1920s mobsters,[11] for him as an uncredited ghost artist.

Now making more money on two pages than his usual weekly salary, Romita accepted the story and continued to ghost for Zakarin on other work.

[14] The work was for Marvel's 1940s forerunner, Timely Comics, which helped give Romita an opportunity to meet editor-in-chief and art director Stan Lee.

[23] The character was billed now as "Captain America, Commie Smasher" in the wake of the Cold War and faced enemies associated with the Soviet Union.

[26] Additionally, Romita would render one of his first original characters, M-11 the Human Robot, in a five-page standalone science-fiction story in Menace #11 (May 1954).

[28] Romita had been recommended to DC's editors by his artist friend Carmine Infantino while serving in the Korean War.

[29] After declining comics sales in the late 1950s forced Atlas to let most of their artists go, Romita transitioned to work for DC exclusively in 1958.

[12] He would "swipe"—an artists' term for using existing work as models, a common practice among novices—from movie stills and from the Milton Caniff comic strip Terry and the Pirates.

[33] Romita's last known DC story work was the six-page "My Heart Tricked Me", inked by Sachs, in Girls' Romances #121 (December 1966), though his spot illustrations, some or all of it reprints of earlier work, continued to appear on one-page "beauty tip" and other filler pages, as well as on letters pages, through early 1970, as did the occasional reprinted story.

His first work for Marvel was inking Jack Kirby's cover and Don Heck's interior pencils on the superhero-team comic The Avengers #23 (December 1965).

He obtained a position at the large ad agency BBDO through his friend Al Normandia, one of the firm's art directors.

[4]Romita began a brief stint on Daredevil beginning with issue #12 (January 1966), initially penciling over Jack Kirby's dynamic layouts as a means of learning Marvel's storytelling house style.

[39] Lee wrote a two-part Daredevil story for issues #16–17 (May–June 1966) with Spider-Man guest starring, to see the character depicted by Romita.

When Ditko abruptly left Marvel after completing The Amazing Spider-Man #38 (July 1966), Lee gave Romita the assignment.

While Romita's depiction of Spider-Man would eventually become the company mascot and the definitive look to the general public, the artist had trepidations: I was hoping against it, believe it or not.

Peter David wrote in 2010 that Romita "made the definitive statement of his arrival by pulling Mary Jane out from behind the oversized potted plant [that blocked the readers' view of her face in issue #25] and placing her on panel in what would instantly become an iconic moment.

"[49] Other characters that debuted in the Lee-Romita era include the Rhino in #41 (October 1966),[50] the Shocker in #46 (March 1967),[51] the Kingpin in #50 (June 1967),[52] and George Stacy in #56 (January 1968).

[58] Cutting back on his Spider-Man workload, Romita began doing only layouts, with finished pencils by Don Heck or Jim Mooney for nearly every issue for a year-and-a-half (#57–75, February 1968 – August 1969).

[60][61][62] Her demise and the Goblin's apparent death one issue later formed a story arc widely considered as the most defining in the history of Spider-Man.

[63] In a June 2017 interview with SyFy Wire, Romita named The Amazing Spider-Man #108 and 109 as the two stories he was proudest of, explaining that by the time he did those issues, he was no longer invoking Steve Ditko, and was asserting his own style as an artist.

[14] In that capacity through at least the late 1980s,[14] Romita played a major role in defining the look of Marvel Comics and in designing new characters.

Feeling this was too simple, Romita made the skull larger to encompass the Punisher's torso, with his belt buckle resembling teeth.

[78] Romita collaborated with The Electric Company and to produce Spidey Super Stories comics, which were aimed at a younger audience and created with help from child psychologists.

[79] In 1976, Romita did uncredited art corrections on the large-format, first DC/Marvel intercompany crossover, Superman vs. the Amazing Spider-Man, over the pencils of Ross Andru.

[80][81] Later that same year, Romita inked Jack Kirby's pencil work on Captain America's Bicentennial Battles, a one-shot story published in an oversized treasury format.

His duties included supervising and hiring other artists, providing corrections and cover sketches when needed, and drawing art for various merchandise.

[92] John Romita Sr. married childhood sweetheart Virginia Bruno in November 1952, who also worked on staff at Marvel as traffic manager from 1975 to 1996.

[86] Romita has been credited with creating a new Spider-Man art style with romance and adventure influences that appealed to an even wider audience.

"[100] While working on DC's romance comics, Romita, finding the stories dull and repetitive, began looking for ways to add more personality into the artwork.

For example, Romita would add flowing hair on women or objects moving in the wind for panels that had little happening and depicting characters from unique angles.