Portrait of Ruin is set in 1944 Europe during World War II,[6] and is a continuation of the story from Castlevania: Bloodlines.

Portrait of Ruin has met with an overall positive critical response and has received high ratings from reviews, along with several awards.

[1] One of the main features to the gameplay is that players can switch freely between two characters, Jonathan and Charlotte, similar to the "Julius mode" from Castlevania: Dawn of Sorrow.

[11] Many enemies from previous Castlevania titles make appearances either as standard monsters or bosses for the sections of the castle and paintings.

Jonathan is the wielder of the legendary whip, "Vampire Killer", which was passed down to him by his father, John Morris from Castlevania: Bloodlines.

As he is not a direct descendant of the Belmont clan, he is unable to unlock the Vampire Killer's full power without the assistance of a member of the Lecarde family.

[14] He disdains humanity because his two real daughters had been killed 30 years prior during World War I. Brauner is able to construct paintings containing pocket dimensions in order to harness the castle's power for his own purposes.

Assisting the two main characters are a priest named Vincent Dorin who acts as a merchant selling weapons, potions, and magic spells, as well as a ghost who introduces himself as "Wind" and provides Jonathan and Charlotte new skills and equipment that once belonged to him if they perform certain tasks called "quests".

Prior to the start of the game, the two sisters, Stella and Loretta travel to Dracula's castle in search of their father, Eric Lecarde.

After the figure transforms into a humanoid male, he explains that he was killed a short time ago and had cast a magical barrier to keep himself conscious while still within the confines of the castle.

Shortly after its defeat, one of the vampire sisters appears and disdains their efforts, saying their control is lessened in only a minor degree.

Both sisters desire to kill the two humans, but Brauner sees Dracula's servant Death as a greater threat, as he could wrest control from him far more easily than them.

Yet, he is gravely disturbed when he sees the statements are true, and promptly leaves to seek a way to destroy Brauner and revive Dracula.

[18] Jonathan and Charlotte encounter Stella at the base of the Tower of Death, and after being promptly defeated, she loses her locket as she flees with her sister.

[20] After searching the castle, Jonathan and Charlotte obtain the Sanctuary spell, a magical attack that dispels curses and allows the dead to rest in peace.

This allows them to regain their sanity, and they subsequently offer to perform a ritual that allows Jonathan to utilize the Vampire Killer whip's full power.

[21] After Jonathan passes the test and defeats the Memory of the Whip, an entity bearing the likeness of Richter Belmont, he is warned against overusing it, as the Vampire Killer drains life force of a non-Belmont wielding the full power, eventually killing the user as it did Jonathan's father.

In an interview with producer Koji Igarashi in June 2006, it was revealed the game would try to utilize the touch screen better than Dawn of Sorrow.

[27] More information concerning online game play were released a month later at Comic-Con 2006, but details on how it would be implemented were still unconfirmed.

[30] The anime style of artwork was retained from Dawn of Sorrow, which Igarashi had switched to in the previous title to appeal more to the younger demographics of the Nintendo handheld systems.

Koji Igarashi stated that the schedule became tight due to Nintendo Wi-Fi difficulties, considering it was their first online enabled game.

The songs "Sandfall" and "In Search of the Secret Spell" that play in the Forgotten City level are originally from Konami's own King's Valley 2 released on the MSX2 computer, composed by Koshiro.

[34] In North America, the official strategy guide was released by BradyGames and featured a complete walkthrough, maps, and item lists.

[48] Dracula was listed as the third top villain of 2006 by Game Informer, citing the final boss fight in Portrait of Ruin as the reason.

[51] IGN stated that "the dramatic score is enough to send a chill up your spine", though mentioned that amount of vocals was sparse.

They also compared it to its predecessor, stating that Portrait of Ruin deviated away from Dawn of Sorrow in terms of gameplay.

They also complimented the online multiplayer, the setting, and the freedom to play the game with or without the DS's special functions, but criticized some of the dialog.

[40] GameSpot called it a great game because it "stays true to the familiar Castlevania design and delivers a fun, lengthy adventure.

"[39] Game Informer mentioned the two character play was "done before, but Portrait of Ruin's system is particularly smooth in execution.