Johns studied a total of three semesters at the University of South Carolina, from 1947 to 1948. He then moved to New York City and studied briefly at the Parsons School of Design in 1949. In 1952 and 1953 he was stationed in Sendai, Japan, during the Korean War.

In 1954, after returning to New York, Johns met Robert Rauschenberg and they became long-term lovers. For a time they lived in the same building as Rachel Rosenthal. In the same period he was strongly influenced by the gay couple Merce Cunningham (a choreographer) and John Cage (a composer). Working together they explored the contemporary art scene, and began developing their ideas on art.

In 1958, gallery owner Leo Castelli discovered Johns while visiting Rauschenberg’s studio. “And we went down,” Castelli remembered. “And then I was confronted with that miraculous array of unprecedented images — flags, red, white and blue… All white… Large ones… small ones, targets… numbers, alphabets. Just an incredible sight… Something one could not imagine, new and out of the blue.” Castelli immediately offered Johns his first solo show. It was here that Alfred Barr, the founding director of New York’s Museum of Modern Art, purchased four works from this show. In 1960 he received the Vincent van Volkmer Prize. In 1963, Johns and Cage founded Foundation for Contemporary Performance Arts, now known as Foundation for Contemporary Arts in New York City.

Since 1960 Johns has worked closely with Universal Limited Art Editions, Inc (ULAE) in a variety of printmaking techniques to investigate and develop existing compositions. Initially, lithography suited Johns and enabled him to create print versions of iconic depictions of flags, maps, and targets that filled his paintings. In 1971, Johns became the first artist at ULAE to use the handfed offset lithographic press, resulting in Decoy — an image realized in printmaking before it was made in drawing or painting. However, apart from the Lead Reliefs series of 1969, he has concentrated his efforts on lithography at Gemini G.E.L. In 1976, Johns partnered with writer Samuel Beckett to create Foirades/Fizzles; the book includes 33 etchings, which revisit an earlier work by Johns and five text fragments by Beckett. He has also worked with Atelier Crommelynck in Paris, in association with Petersburg Press of London and New York; and Simca Print Artists in New York. In 2000, Johns produced a limited-edition linocut for the Grenfell Press.

For decades Johns worked with others to raise both funds and attention for Merce Cunningham’s choreography. He privately assisted Robert Rauschenberg in some of his 1950s designs for Cunningham. In spring 1963, Johns helped start the Foundation for Contemporary Performance Arts, then intended to sponsor and raise funds in the performance field; the other founders were John Cage, Elaine de Kooning, the designer David Hayes, and the theater producer Lewis B. Lloyd. Johns later was the Merce Cunningham Dance Company’s artistic adviser from 1967 to 1980. In 1968 Johns and Cunningham made a Duchamp-inspired theater piece, Walkaround Time, in which Johns’s décor replicates elements of Duchamp’s work The Large Glass (1915–23). Earlier, Johns also wrote neodada lyrics for The Druds, a short-lived avant-garde noise music art band that featured prominent members of the New York proto-conceptual art and minimal art community.

In 1964, architect Philip Johnson, a friend, commissioned Johns to make a piece for what is now the David H. Koch Theater at Lincoln Center. After presiding over the theatre’s lobby for 35 years, Numbers (1964), an enormous 9-foot-by-7-foot grid of numerals, was supposed to be sold by the center for a reported $15 million. Art historians consider Numbers a historically important work in part because it is the largest of the artist’s numbers motifs and the only one where each unit is on a separate stretcher, fashioned from a material called Sculpmetal, which was chosen by the artist for its durability. Responding to widespread criticism, the board of Lincoln Center had to drop its selling plans.

Johns currently lives in Sharon, Connecticut, and on the island of Saint Martin. Until 2012, he lived in a rustic 1930s farmhouse with a glass-walled studio in Stony Point, New York. He first began visiting Saint Martin in the late 1960s and bought the property there in 1972. The architect Philip Johnson is the principal designer of his Saint Martin home, a long, white, rectangular structure divided into three distinct sections.

In 1973, Johns produced a print called Cup 2 Picasso, for XXe siècle, a French publication. For the May 2014 issue of Art in America, he created a black-and-white lithograph depicting many of his signature motifs, including numbers, a map of the United States and sign language.

In 1980 the Whitney Museum of American Art paid $1 million for Three Flags (1958), then the highest price ever paid for the work of a living artist. In 1988, Johns’ False Start was sold at auction at Sotheby’s to Samuel I. Newhouse, Jr. for $17.05 million, setting a record at the time as the highest price paid for a work by a living artist at auction, and the second highest price paid for an artwork at auction in the U.S. In 2006, private collectors Anne and Kenneth Griffin (founder of the Chicago-based hedge fund Citadel LLC) bought False Start (1959) from David Geffen for $80 million, making it the most expensive painting by a living artist. On November 11, 2014, a 1983 version of Flag was auctioned at Sotheby’s in New York for $36 million, establishing a new auction record for Johns.

Johns was elected a Fellow of the American Academy of Arts and Sciences in 1984. In 1990, he was awarded the National Medal of Arts. On February 15, 2011 he received the Presidential Medal of Freedom from President Barack Obama, becoming the first painter or sculptor to receive a Presidential Medal of Freedom since Alexander Calder in 1977. In 1990 he was elected into the National Academy of Design as an Associate member and became a full Academician in 1994. In 1994 he was awarded the Edward MacDowell Medal.

In 1998, the Metropolitan Museum of Art in New York bought Johns’ White Flag. While the Museum would not disclose how much was paid, The New York Times reported that “experts estimate [the painting’s] value at more than $20 million”. The National Gallery of Art acquired about 1,700 of Johns’ proofs in 2007. This made the gallery home to the largest number of Johns’ works held by a single institution. The exhibition showed works from many points in Johns’ career, including recent proofs of his prints. The Greenville County Museum of Art in Greenville, South Carolina, has several of his pieces in their permanent collection.

The most expensive work sold of Jasper Johns was Flag (1958), one of a series, was sold privately to hedge fund billionaire Steven A. Cohen in 2010 for a reported $110 million (then £73 million; €81.7 million). The seller was Jean-Christophe Castelli, son of Leo Castelli, Johns’s legendary dealer, who had died in 1999. While the price was not disclosed by the parties, art experts say Cohen paid about $110 million. “Flags” are Johns’s most famous works. The artist painted his first American flag in 1954–55, a work now at the MoMA.