In 1799, Constable persuaded his father to let him pursue a career in art, and Golding granted him a small allowance. Entering the Royal Academy Schools as a probationer, he attended life classes and anatomical dissections, and studied and copied old masters. Among works that particularly inspired him during this period were paintings by Thomas Gainsborough, Claude Lorrain, Peter Paul Rubens, Annibale Carracci and Jacob van Ruisdael. He also read widely among poetry and sermons, and later proved a notably articulate artist.

In 1802 he refused the position of drawing master at Great Marlow Military College (now Sandhurst), a move which Benjamin West (then master of the RA) counselled would mean the end of his career. In that year, Constable wrote a letter to John Dunthorne in which he spelled out his determination to become a professional landscape painter:

By 1803, he was exhibiting paintings at the Royal Academy. In April he spent almost a month aboard the East Indiaman Coutts as it visited south-east ports while sailing from London to Deal before leaving for China.

In 1806 Constable undertook a two-month tour of the Lake District. He told his friend and biographer, Charles Leslie, that the solitude of the mountains oppressed his spirits, and Leslie wrote:

From 1809, his childhood friendship with Maria Elizabeth Bicknell developed into a deep, mutual love. Their marriage in 1816 when Constable was 40 was opposed by Maria’s grandfather, Dr Rhudde, rector of East Bergholt. He considered the Constables his social inferiors and threatened Maria with disinheritance. Maria’s father, Charles Bicknell, solicitor to King George IV and the Admiralty, was reluctant to see Maria throw away her inheritance. Maria pointed out to John that a penniless marriage would detract from any chances he had of making a career in painting. Golding and Ann Constable, while approving the match, held out no prospect of supporting the marriage until Constable was financially secure. After they died in quick succession, Constable inherited a fifth share in the family business.

Constable adopted a routine of spending winter in London and painting at East Bergholt in summer. In 1811 he first visited John Fisher and his family in Salisbury, a city whose cathedral and surrounding landscape were to inspire some of his greatest paintings.

Another source of income was country house painting. In 1816, he was commissioned by Major-General Francis Slater-Rebow to paint his country home, Wivenhoe Park, Essex. The Major-General also commissioned a smaller painting of the fishing lodge in the grounds of Alresford Hall, which is now in the National Gallery of Victoria. Constable used the money from these commissions towards his wedding with Maria Bicknell.

John and Maria’s marriage in October 1816 at St Martin-in-the-Fields (with Fisher officiating) was followed by time at Fisher’s vicarage and a honeymoon tour of the south coast. The sea at Weymouth and Brighton stimulated Constable to develop new techniques of brilliant colour and vivacious brushwork. At the same time, a greater emotional range began to be expressed in his art.

The picture was Flatford Mill (Scene on a Navigable River), it was the largest canvas of a working scene on the River Stour that he had worked on to date and the largest he would ever complete largely outdoors. Constable was determined to paint on a larger scale, his objective was not only to attract more attention at the Royal Academy exhibitions but also, it seems, to project his ideas about landscape on a scale more in keeping with the achievements of the classical landscape painters he so admired. Although Flatford Mill failed to find a buyer when it was exhibited at the Royal Academy in 1817. Its fine and intricate execution drew much praise, encouraging Constable to move on to the even larger canvases that were to follow.

In 1821, his most famous painting The Hay Wain was shown at the Royal Academy’s exhibition. Although it failed to find a buyer, It was viewed by some important people of the time, including two Frenchmen, the artist Théodore Gericault and writer Charles Nodier. According to the painter Eugène Delacroix, Géricault returned to France ’quite stunned‘ by Constable’s painting. While Nodier suggested French artists should also look to nature rather than relying on trips to Rome for inspiration. It was eventually purchased, along with View on the Stour near Dedham, by the Anglo-French dealer John Arrowsmith, in 1824. A small painting of Yarmouth Jetty was added to the bargain by Constable, with the sale totalling £250. Both paintings were exhibited at the Paris Salon that year, where they caused a sensation, with the Hay Wain being awarded a gold medal by Charles X.

To the sky studies he added notes, often on the back of the sketches, of the prevailing weather conditions, direction of light, and time of day, believing that the sky was “the key note, the standard of scale, and the chief organ of sentiment” in a landscape painting. In this habit he is known to have been influenced by the pioneering work of the meteorologist Luke Howard on the classification of clouds; Constable’s annotations of his own copy of Researches About Atmospheric Phaenomena by Thomas Forster show him to have been fully abreast of meteorological terminology. “I have done a good deal of skying”, Constable wrote to Fisher on 23 October 1821; “I am determined to conquer all difficulties, and that most arduous one among the rest”.

Constable’s pleasure at his own success was dampened after his wife started displaying symptoms of Tuberculosis. Her growing illness meant that Constable took lodgings for his family in Brighton from 1824 until 1828, in the hope the sea air could restore her health. During this period Constable split his time between Charlotte Street in London and Brighton. This change saw Constable move away from large scale Stour scenes in favour of coastal scenes. He continued painting six foot canvases, although he was initially unsure of the suitability of Brighton as a subject for painting. In a letter to Fisher in 1824 he wrote

A number of distractions meant that The Lock wasn’t finished in time for the 1823 exhibition, leaving the much smaller Salisbury Cathedral from the Bishop’s Grounds as the artists main entry. This may have occurred after Fisher forwarded Constable the money for the painting. This both helped him out of a financial difficulty and nudged him along to get the painting done. The Lock was therefore exhibited the following year to more fanfare and sold for 150 Guineas on the first day of the exhibition, the only Constable ever to do so. The Lock is the only upright landscape of the Stour series and the only six footer that Constable painted more than one version of. A second version now known as the ‘Foster version’ was painted in 1825 and kept by the artist to send to exhibitions. A third, landscape version, known as ‘A Boat passing a Lock’ (1826) is now in the collection of the Royal Academy of Arts.. Constable’s final attempt, The Leaping Horse, was the only six-footer from the Stour series that didn’t sell in Constable’s lifetime.

In his lifetime, Constable sold only 20 paintings in England, but in France he sold more than 20 in just a few years. Despite this, he refused all invitations to travel internationally to promote his work, writing to Francis Darby: “I would rather be a poor man [in England] than a rich man abroad.” In 1825, perhaps due partly to the worry of his wife’s ill-health, the uncongeniality of living in Brighton (“Piccadilly by the Seaside”), and the pressure of numerous outstanding commissions, he quarreled with Arrowsmith and lost his French outlet.

Chain Pier, Brighton was his only ambitious six-foot painting of a Brighton subject, it was exhibited in 1827. The Constable’s persevered in Brighton for five years to aid Maria’s health, but to no avail. After the birth of their seventh child in January 1828, they returned to Hampstead where Maria died on 23 November at the age of 41. Intensely saddened, Constable wrote to his brother Golding, “hourly do I feel the loss of my departed Angel—God only knows how my children will be brought up…the face of the World is totally changed to me”.

He was elected to the Royal Academy in February 1829, at the age of 52. In 1831 he was appointed Visitor at the Royal Academy, where he seems to have been popular with the students.

In 1835, his last lecture to students of the Royal Academy, in which he praised Raphael and called the Academy the “cradle of British art”, was “cheered most heartily”. He died on the night of 31 March 1837, apparently from heart failure, and was buried with Maria in the graveyard of St John-at-Hampstead Church in Hampstead in London. (His children John Charles Constable and Charles Golding Constable are also buried in this family tomb.)

Constable’s watercolours were also remarkably free for their time: the almost mystical Stonehenge, 1835, with its double rainbow, is often considered to be one of the greatest watercolours ever painted. When he exhibited it in 1836, Constable appended a text to the title: “The mysterious monument of Stonehenge, standing remote on a bare and boundless heath, as much unconnected with the events of past ages as it is with the uses of the present, carries you back beyond all historical records into the obscurity of a totally unknown period.”

In 2019 two drawings by Constable were unearthed in a dusty cardboard-box filled with drawings; the drawings sold for £60,000 and £32,000 at auction.