Few museums have a richer or more tortuously unusual history than the Dulwich Picture Gallery. The museum is well known for its rich holdings of Old Master painting: seven Poussins, three Rembrandts, four Murillos, works by Rubens and Van Dyck and many important Italian pictures. Less well known is the fact that most of those are the fruits of a single extraordinary bequest, blown in the direction of Dulwich by the fickle winds of history.

In the late eighteenth century, two picture dealers, Peter Francis Bourgeois and Noel Desenfans, were employed by King Stanislaus II of Poland to create a great royal collection for his palace in Warsaw. Thanks to the French Revolution and the humbling of the French aristocracy, extraordinary works of art were available at knockdown prices. Bourgeois and Desenfans acquired a remarkable hoard of masterpieces for their Polish client. But before he could pay for them he had been deposed from the throne by an occupying Russian army.

The core of that great collection, some 370 works, was eventually bequeathed by Francis Bourgeois to Dulwich College, which was at the time a rather sleepy private shool for boys in South London. Remarkably, the governors of the school rose to the challenge. Sir John Soane was employed to design a beautiful, small, purpose-built museum to house the new bequest. The Dulwich Picture Gallery, the first public picture gallery in England, opened its doors in 1811.

Antoni Malinowski, a London-based Polish artist, reflects on this unique concatenation of events in his installation, “The Polish Connection”, which currently occupies one large room at the heart of Soane’s building. The display juxtaposes a remarkable group of portraits of King Stanislaus II of Poland, borrowed from the Royal Castle and National Museum in Warsaw, with a large wall drawing by Malinowski himself.

The pictures from Poland are well worth seeing in their own right, flamboyant essays in the pomp of late Baroque state portraiture. The weak-jawed and watery-eyed king – Poland’s last – is wrapped in a hundred yards of crimson drapery and resplendent in a suit of silver thread. He looks out across the suite of galleries as if to survey all the works of art that could have been his, had history turned out differently.

Malinowski’s drawing, by contrast, consists of a hesitant and slightly ascetic welter of marks. Black lines climb a white wall. The effect is of an enigmatic, elegiac semaphore. This is presumably a conceptualist’s metaphor for the strange case of King Stanislaus and his art – the abstract re-enactment of a gesture which, while intended to produce one particular outcome in Poland, resulted in something  utterly different taking place thousands of miles away in London.

The main exhibition at Dulwich Picture Gallery over the summer focusses on a different aspect of the museum’s holdings. “The Best of British”, which occupies the principal temporary exhibition space, focusses on the often overlooked British collections, including many pictures only rarely shown in the main galleries.

The display serves as a reminder that Dulwich’s collection as a whole predates the acquisition of King Stanislaus’s paintings. By the last quarter of seventeenth century, Dulwich College was already in possession of two other art collections. Edward Alleyn and William Cartwright, both actors, had bequeathed their pictures to the school (it may well have been the presence of their pictures in Dulwich that gave Francis Bourgeois the idea of his later and larger bequest). As Ian Dejardin notes in his preface to John Ingamell’s new Catalogue of the British Paintings in the Dulwich picture Gallery, “there are no outright masterpieces in the two actors’ collections; their interest lies in the simple fact of their existence – two aspirational collections put together by non-aristocrats in the entertainment business intent on bettering their perceived standing in the world.”

Edward Alleyn, who founded Dulwich College in the first place,  probably wanted his pictures to be used as educational tools. They are portraits of British kings, queens and other worthies, painted by jobbing artists of no great distinction during the early years of the seventeenth century. But these glass-eyed regal dummies, these wreathed portraits of poets, such as the Dante, are fascinating nonetheless. They are rare survivals of a largely lost folk art tradition – relics of a genuinely popular form of painting that survived and thrived, in post-Reformation Britain.

The Alleyn bequest is also notable for a small but suggestively romantic collection of portraits of English actors. Some of the most suggestive are anonymous pictures of anonymous thespians. Anon’s Portrait of a Man is so vivid that it seems unexpectedly contemporary – bleary-eyed and red of face, he might easily be mistaken for Kenneth Branagh in character as some drunken loon in a Jacobean drama. Another work by Anon, Richard Burbage, is less impressive as a work of art, but memorable as a relic nonetheless. This whey-faced mannequin in a white collar was the first actor to play Hamlet, Lear, Richard III and Othello.

William Cartwright’s bequest to Dulwich added some other memorable curiosities to the Dulwich collections, including that strange and sombre funerary image, The Judde Memorial. The pallid corpse of the deceased lies wrapped in grave clothes, while his relations remember him by touching fingers across the cranium of a Yorick-like skull. An inscription beneath offers the counsel “Live to Die: And Die to Live”.

But the most remarkable group of English pictures ever given to Dulwich were contained in the Linley Bequest of 1835. These include Gainsborough’s immortally haunting portrait of The Linley Sisters, as well as a small pair of portraits of their brothers and father, also by Gainsborough, and related family paintings by Thomas Lawrence, Archer James Oliver and James Lonsdale. For the occasion of the Dulwich summer show, all have been gathered together in a single room, where they form a poignant collective portrait of a single English family.

The display tells the story of the fate that befell each of Linleys, a tale of tragedy heaped on tragedy. The girls married men of the theatre, who let them down, exploited them and led them to early graves. The lives of the boys, one of whom was by common consent destined to be “the English Mozart”, were cut short by disease and freakish accident. It seems deeply appropriate that Gainsborough, who was so alive to the fleeting qualities of light, and who was so responsive to the transience of human identity itself, with its flashes and gleams of character or feeling, should have been the principal chronicler of this singularly sad family story.