Wingard was born in Oak Ridge, Tennessee and graduated from Full Sail University in 2002. His first feature, the horror comedy Home Sick, starring Bill Moseley and Tiffany Shepis, proved to be a stepping stone to his second feature, the psychotropic ghost story horror film Pop Skull. Made on a total budget of $2,000, Pop Skull had its international premiere at the Rome Film Festival and its domestic premiere at the AFI Film Festival in 2007. A Horrible Way to Die (2010) and What Fun We Were Having (2011) followed.

In 2011, Wingard co-directed Autoerotic with mumblecore icon (and frequent actor in Wingard films) Joe Swanberg. He was selected to direct one chapter of The ABCs of Death, a 26-chapter horror comedy anthology for Drafthouse Films and Magnet. A solo directorial effort, You’re Next, a home invasion slasher, premiered at the 2011 Toronto International Film Festival as part of the ‘Midnight Madness’ section. The film was acquired by Lionsgate, and received a wide release in August 2013 to generally favorable reviews.

In 2014, Wingard directed The Guest starring Dan Stevens, which premiered at the Sundance Film Festival, the Toronto International Film Festival and Fantastic Fest, receiving wide critical acclaim upon its wider theatrical release in mid-September. Wingard directed Lionsgate’s horror film Blair Witch, based on a script by Simon Barrett. The film is a sequel to the 1999 found footage horror classic The Blair Witch Project and received mostly ambivalent reviews.

In 2015, Wingard signed on to direct a live action American film adaptation of Tsugumi Ohba and Takeshi Obata’s popular horror crime-thriller manga series Death Note. The neo-noir dark fantasy horror-thriller was released on Netflix on August 25, 2017, to a mixed reception, with criticism aimed at the number of changes from the source material, rushed plot, shallow execution, writing and pacing- while praise was aimed at the visual style, direction, performances of the cast, soundtrack and the dark, macabre sense of humour, along with the attempted unique and distinctive take on the Death Note mythos.

In May 2017, Wingard was announced as the director for Godzilla vs. Kong, which is slated for release in May 2021.