During a dark time in the Heian period, when evil forces threaten the kingdom, the emperor relies on the onmyōji to keep the supernatural forces in line. But as political events become highly charged, friction within the order leads to betrayal. Now, Seimei, a talented member of the clan, must face down his master, Dōson, in the hopes of restoring peace to the kingdom.

平安时代，百鬼夜行，封鬼仪式正在右大臣藤原安麻吕府邸进行。安麻吕之女日美子（深田恭子 饰）戎装登场，一箭命中靶心，引来全场惊叹。这位被喻为“连鬼都不敢接近”的公主，却令源博雅（伊藤英明 饰）暗自倾心。天现异象，京都骚动，魍魉横行。平安京已有四人遇害，民间出现驱鬼术士幻角（中井贵一 饰），日美子亦在异象后开始梦游。博雅为此替右大臣来请安倍晴明（野村万斋 饰）商谈。与此同时，宫廷供奉的出云三神器之一草薙剑也出现了异动。晴明受天皇所托，与博雅开始调查种种异况背后出云与大和的隐秘渊源。
博雅和夜弹琵琶的神秘少年须佐（市原隼人 饰）相识为乐友，须佐负伤被日美子所救，三人在右大臣府邸相逢。同一时刻，右大臣主动找到晴明，坦白了十八年前天现异象时，大和攻打出云的事实……
本片为电影《阴阳师》续作。