Although the painting is sometimes called Ivan the Terrible kills his son, Repin did not paint the moment at which the Tsar hits the Tsarevich. The work does not represent violence but its resolution. Ivan the Terrible holds his son. His eyes "bulging with horror, despair and madness", he embraces him by the waist. Tsarevich Ivan, weeping, gently waves his hand.

Two modifications to the preliminary sketches show the distance established by the painter with the altercation; the sceptre with which the Tsar strikes his son's temple is in his hand in the first sketches while in the final painting, it is on the floor in front of them. The bloodstain where the Tsarevich's head rests on the floor, which is very visible in the oil sketch Repin made in 1883, and which he kept and resumed later, is erased in the shadows of the final painting. Ivan Ivanovich's dress no longer has a long bloodstain. The represented moment becomes one of remorse, forgiveness and love. The painting also shows, in its centre, the reality and the irreversibility of the tsar's act: the blood flows from his son's temple and the attempt Ivan the Terrible makes to contain it with his left hand is hopeless.

The painting's 199.5 cm × 254 cm (78.5 in × 100.0 in) canvas is one of Repin's largest works; its dimensions are comparable to those of the Barge Haulers on the Volga and the Religious Procession in Kursk Governorate.

The two characters are crisscrossed with each other in the centre of the painting. They are depicted in a twilight and stand out from both the foreground of the canvas and the darker background. The gesture with which Ivan the Terrible hugs and supports his son's waist is reminiscent of the paintings The Return of the Prodigal Son and David and Jonathan (Rembrandt) by Dutch painter Rembrandt, which Repin studied and admired since his formative years, and are housed in the Hermitage Museum.

The construction of the painting is based on objects and pieces of furniture that are distributed around the characters: the crumpled red carpets on the floor, the Tsarevich's boots, the sceptre, the throne that was overturned during the argument, one of the ornamental balls that sparkles at the level of the son's eyes, and his cushion. Behind the figures, other pieces of furniture, such as the stove, the mirror of the Armor Museum and the chest of the Rumyantsev Palace, are less discernible. The back wall of the room is partly covered with a red-and-black diamond pattern. At the top left is a narrow bay.

Repin wrote he refused "the acrobatics of the brush and painting for the sake of painting" and that "the beauty, the touch or the virtuosity of the brush" was not the only important things because he had always pursued "the essential: the body, as a body". Ivan the Terrible and his Son Ivan is "painted with such a diversity of craftsmanship and with such a rich palette of dark chords" that it is, according to Russian painter and art critic Ivan Kramskoi, an "authentic orchestra". An "intense red" or "blood red", and "thick and saturated crimson red" predominates. It is painted with pure colour, with no additions, and then reworked by the painter with an extraordinary diversity of shades.

The scarlet red of the blood flowing from the wound on the Tsarevich's temple stands out, as do the reflections on the folds of his kaftan, and finally the dark-red puddle of blood on the red carpet, and this tension of colours resonates with the tragedy depicted on the canvas. In the centre, the magnificence of the Tsarevich's kaftan contrasts with the darkness of Ivan the Terrible's black coat. Repin breaks this combination of blood red, pink and dark-brown tones with the complementary tones of the green of the Tsarevich's boots and the deep-blue of his velvet trousers. White light, "cold and weak", which penetrates through a narrow bay, attenuates this tension of colours and further reinforces the dramatic tension of the scene.

For Repin and his contemporaries, the painting's first symbolic function is to express the existence of violence and moral rejection, which must be the object. According to Ivan Kramskoi; "it seems that a human being, after having carefully looked at this painting, even if only once, will be forever protected from the wild beast he has, as they say, in him".

The representation of the aftermath of the father's altercation with his son is a historical episode and illustrates a person's "eternal" capacity to physically harm their neighbour. The painting can be understood as a pictorial parable of the commandment "Thou shalt not kill".

The picture also seemed to approach a more-particularly religious inspiration, showing "Christian love and forgiveness" can repair crime, even infanticide. The tsarevich's gesture and face are "almost like that of an icon", the tear that runs down the wing of his nose seem to depict forgiveness. The similarity of the gesture of Ivan the Terrible's right arm with those of the figures in the two Rembrandt paintings also aligns with this position.

In the interpretation of the work, the personality of the writer Vsevolod Garshin provides additional details. In this period, Repin used Garshin as a model in several other paintings, including Portrait [fr] (1884) and the large painting They Did Not Expect Him, in which Garshin poses for the main character. Work on They Did Not Expect Him began in 1884 and ended the year of Garshin's suicide in 1888.

Repin appreciated Vsevolod Garshin, whom he considered an "incarnation of the divine" during their friendship and after his death. He wrote "his pensive eyes, often mixed with tears provoked by some injustice, his humble and delicate attitude, his angelic personality, with the purity of a dove, were those of a God". Repin's painting refers to Garshin's physical features, his personality and his deeply peaceful thought.

The political significance of the painting cannot be eluded because of the reactions to which it was immediately the subject. Repin combined Ivan the Terrible's killing of his son with the assassination of Alexander II. Neither Repin nor Russian art critics expanded upon this point.

French critics wrote about the point. According to Alain Besançon, the tsarevich's murder by the tsar is a central scene of the Russian myth, which Repin was the first to represent: the history of Russia would be built on the sacrifice of sons killed by their fathers.

Pierre Gonneau supports a converging position, stressing this sacrificial vision refers "to the symbolic roots of the monarchy because the sacrificed tsarevich finds himself in a position to embody the forces opposing the authority of the tsar". It makes a link with the trial of Tsarevich Alexis, son of Peter the Great, and his death as a result of torture. This other conflict between a father and his son is the theme of Nikolai Ge's 1871 painting Peter the Great interrogates Tsarevich Alexis in Peterhof [ru].

In 1909, on a commission from the industrialist and collector Stepan Ryabushinsky [ru], Repin painted a second version of Ivan the Terrible and His Son Ivan, which he called Filicide (Сыноубийца). It is on display at Voronezh Museum of Fine Arts. The second version was painted 25 years later than the first. In this version, Repin added a female character in the background and unveiled more colours than in the original painting, taking it in a more "luxuriant" direction, while Tsar Ivan's face is collapsed in grief.

• 
  Filicide (1909).
• 
  Detail of Filicide.

In 1885, Ivan the Terrible and His Son Ivan was shown for the first time to Repin's painter friends, among whom were Ivan Kramskoi, Ivan Shishkin, Nikolai Yaroshenko and Pavel Brullov. According to Repin, his hosts were stunned and silent for a long time, waiting to see what Kramskoi would say:

I was seized with a feeling of complete appreciation for Repin. There it is, the thing, what a level of talent ... And how it's painted, my God, how it's painted! ... And what is this murder, carried out by a wild beast and a psychopath? ... A father hits his son with his sceptre in the temple? One moment ... He utters a cry of terror ... He grabs him, he sits him on the ground, he raises him ... He presses one of his hands on the wound in the temple (and blood gushes out of the cracks between the fingers) ... and as he bawls ... It's an animal, howling with fear ... the very spot that the son has marked with his temple ... Really, this scene is drowning us in half-light and a kind of natural tragic.

— Ivan Kramskoi

The very conservative Attorney General of the Holy Synod Konstantin Pobedonostsev told Alexander III of his "repulsion" and perplexity about the painting, which did not please the Tsar and his entourage, and on 1 April 1885, viewings of the painting were forbidden. It was the first painting to be censored in the Russian Empire, and Pavel Tretyakov, who bought it, was told "not to expose it, and more generally not to allow it to be brought to the attention of the public by any other means". The ban was lifted on 11 July 1885 after the intervention of the painter Alexey Bogolyubov.