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Kayvan Novak as Nandor the Relentless – Once the bloodthirsty leader of the fictional kingdom of Al-Quolanudar in southern Iran and a warrior serving the Ottoman Empire. At age 760, he is the oldest of the group and their self-proclaimed leader, though it is obvious he has little to no authority. Although he genuinely cares for his human familiar Guillermo, he has difficulty expressing it. Nandor is also quite naïve to the ways of modern society and humans, which often results in Guillermo becoming frustrated with him.

Matt Berry as Leslie "Laszlo" Cravensworth – A 310-year-old vampire from British nobility who was turned by Nadja and is now married to her. A pansexual and former porn actor who is often preoccupied with sexual thoughts, he enjoys sexual encounters with both Nadja and Nandor. His interests are more varied and intellectual than the other characters. He frequently performs scientific experiments on the humans killed by him and the other vampires. According to Nadja, he once forgot to eat for an extended period of time because he was "writing poetry and wanking". He and Nadja were at one time prolific songwriters, and, it seems, wrote what eventually became "Row, Row, Row Your Boat", "Come on Eileen" and "Kokomo". Laszlo also enjoys making topiary sculptures of vulvas in the yard, including those of his wife, and mother.

Natasia Demetriou as Nadja of Antipaxos – A 500-year-old Greek Romani vampire who turned Laszlo into a vampire and later married him. Abrasive and aggressive, she is frequently frustrated with her male housemates and nostalgic about her human life. The only character she shows any affection for is Laszlo, often wrathfully lashing out at Guillermo. She has entertained an affair with a reincarnated knight named Gregor for hundreds of years, only for him to be decapitated in every reincarnation. She later becomes manager of her own vampire nightclub.

Demetriou also plays Nadja's human ghost, split from its corporeal form when Nadja was turned into a vampire, who inhabits a doll which has appeared since the second season.

Harvey Guillén as Guillermo de la Cruz – Nandor's long-suffering Latino familiar. Despite his frustration with his unreasonable workload and Nandor's disregard for his mortality, he has served his master for more than a decade in the hope of being made a vampire. Guillermo discovers that he is a descendant of the famous vampire hunter Abraham Van Helsing and proves to be very skilled at killing vampires, giving him conflicting feelings about his desire to become a vampire. Guillermo's skill as a vampire slayer leads to him becoming a bodyguard for Nandor, Nadja, and Laszlo. He comes out as gay to his family but reveals his desire to become a vampire at the same time, prompting Nadja to erase their memories of his confession.

Mark Proksch as Colin Robinson (and Baby Colin / "The Boy") – An energy vampire who lives in the basement. He sustains himself by draining humans and fellow vampires of their life force by being extremely boring or frustrating. As a "day walker", he is not harmed by sunlight or entry into churches, and thus holds a regular job in an office where he feeds on his coworkers' frustrations. This also means that he financially supports the group. Unlike the others, he shows no outward signs of vampirism and appears as a regular human, with the only hints being his glowing irises and demonic facial expression when he feeds on energy, and his reflection showing a pale and decrepit version of himself. Following his 100th birthday, he dies and his infant offspring bursts out of his chest. Having rapidly grown to adulthood, Colin Robinson's son discovers a hidden room filled with Colin Robinson's diaries and regains Colin Robinson's memories as a result, forgetting his time as a child and essentially becoming a reincarnation of Colin Robinson.

Kristen Schaal as The Guide (also known as the "Floating Woman") – An envoy of the Vampiric Council who is able to teleport short distances and sometimes speaks in a demonic voice. She frequently expresses her desire to be socially accepted by the other vampires, yet is almost always rejected. She later works for Nadja as the latter turns the Vampiric Council's headquarters into a nightclub. (seasons 5–6; guest season 1; recurring seasons 3–4)

Recurring

Doug Jones as Baron Afanas – An ancient vampire from the Old Country who believes vampires should rule the world. Both Nadja and Laszlo had secret affairs with the Baron despite his lack of genitals. Later it is disclosed that he is not actually a Baron, but simply "barren" because he was unable to have children. In the first season, Guillermo inadvertently kills the Baron by opening a door and exposing him to sunlight. In the third season, however, it is revealed that he barely survived, albeit reduced to his head, torso and left arm. In later seasons, The Baron chooses to live a quaint, suburban lifestyle with The Sire, another legendary vampire. (seasons 1, 3–6)

Anthony Atamanuik as Sean Rinaldi – The human next-door neighbor. He sometimes witnesses Laszlo doing something vampiric but is easily hypnotized into forgetting everything. The vampires spare him because he brings their trash cans in when they forget, and Laszlo considers Sean his best friend. In season 5, it's implied that Sean is slowly, yet consistently, becoming dumber due to experiencing a constant stream of hypnosis and his rampant alcoholism.

Beanie Feldstein as Jenna – a LARPer and virgin whom Guillermo lured for the vampires to feast on. She was later transformed into a vampire by Nadja who witnessed her being treated poorly by her peers. During her vampire training with Nadja, she discovers she has the rare ability to turn invisible, which fits the tendency of people to ignore her, yet she struggles with turning into a bat. (season 1)

Veronika Slowikowska as Shanice – Jenna's college roommate who witnesses her transformation into a vampire. Shanice later joins the Mosquito Collectors of the Tri-State Area, a secret team of amateur vampire hunters. (seasons 1–2)

Nick Kroll as Simon the Devious – A vampire who rules over the Manhattan vampires and owns the Sassy Cat nightclub. He was initially a close friend to the Staten Island vampires when they first arrived in America, but he quickly became their shared enemy thanks to his willingness to trick and betray the trio. He is obsessed with Laszlo's cursed hat made out of witch skin and is often surrounded by a posse of vampires called "The Leatherskins". (guest seasons 1–2, 4)

Jake McDorman as Jeff Suckler – A reincarnation of Nadja's former human lover, Gregor, a knight who has been killed by decapitation in each of his lives. Nadja eventually restores Jeff's memories of his previous lives so that he can be more like his former self, leading to him falling into insanity and being committed to a mental institution. It is later revealed to Nadja and Gregor that Laszlo had been causing each of his deaths throughout history, which he does again. (season 1; guest season 2)

Vanessa Bayer as Evie Russell – Colin Robinson's co-worker. He discovers that she is an advanced form of energy vampire — an emotional vampire — who feeds off of the pity and sadness generated by her outlandish stories of suffering and misfortune. She and Colin Robinson date for a short time, feeding together on bored and pitying humans until he begins to feel the relationship is unhealthy. In season 5, she becomes Staten Island's City Comptroller, taking over for Colin Robinson's campaign after he intentionally exposed his penis in a video meeting. Her first name is a homophone of "E.V.", for Emotional Vampire. (guest seasons 1, 5)

Marceline Hugot as Barbara Lazarro – The president of the Staten Island Council. She was going to be the vampires' way of taking over Staten Island until Laszlo left a pile of dead raccoons on her doorstep in an attempt to win her trust, resulting in her believing it was a form of terrorist threat. She later appears running against Colin Robinson in the comptroller election. (guest seasons 1, 5)

Chris Sandiford as Derek – A vampire hunter turned vampire and convenience store clerk. (seasons 2–5, guest season 6)

Myrna Cabello as Silvia de la Cruz – Guillermo's mother (seasons 2, 4–5)

Haley Joel Osment as Topher – Nadja and Laszlo's familiar who is accidentally killed and revived as a zombie. Unlike Guillermo, Topher has no interest in becoming a vampire. He is energetic, fun-loving, and charismatic, and he is well-liked by all other members of the household, except Guillermo. (guest seasons 2, 5)

Benedict Wong as Wallace – A necromancer and tchotchke salesman whom Lazlo views as a fraud and con artist and often feuds with him. (guest seasons 2, 5)

Marissa Jaret Winokur as Charmaine Rinaldi – Sean's wife. (guest seasons 2–6)

Anoop Desai as Djinn – Nandor's magical genie, who is indebted to grant him a large number of wishes. (season 4; guest season 5)

Parisa Fakhri as Marwa – Nandor's resurrected ex-wife, now fiancée (season 4, guest season 6)

Frankie Quiñones as Miguel – Guillermo's cousin (guest seasons 4–6)

Mike O'Brien as Jerry the Vampire – The house's fifth roommate who has been in a "super slumber" since 1976, and intended to be awoken on New Year's Eve, 1996. (season 6)

Tim Heidecker as Jordan – Senior partner at Cannon Capital Strategies, the private equity firm where Guillermo, Nadja, and Nandor have been hired. (season 6)

Andy Assaf as Cravensworth's Monster – A Frankenstein-like creature assembled and animated by Laszlo. (season 6)

Guests

Arj Barker as Arjan – The pack leader of the Staten Island Werewolf Support Group. He entered into a truce between his kind and the vampires (which was created in 1993).

Dave Bautista and Alexandra Henrikson as Garrett and Vasillika the Defiler – A duo of vampires imprisoned by the council after Garrett was framed by Laszlo for turning a baby into a vampire (which is very illegal), and Vasillika for too much defiling.

Mary Gillis as June – Nadja and Laszlo's familiar. She appears to be an ill old woman who communicates through grunts. She is killed when the Baron sucks all her blood when he arrives on Staten Island.

Jeremy O. Harris as Colby – A human familiar to Dantos the Cruel and Radinka the Brutal, two 400-year-old vampires who appear to be children while Colby portrays as their father.

Gloria Laino as The Baron's Familiar – The Baron's familiar, who maintains a silent, watchful eye on the vampires of Staten Island as her master awakes. Guillermo says that she pops out of nowhere and hears "everything".

Paul Reubens as Paul – A member of the council.

Tilda Swinton as a fictionalized version of herself who is the leader of the Vampiric Council.

Wesley Snipes as Wesley the Daywalker / Wesley Sykes – A half-vampire member of the Council who could not participate in person but only video chat through Skype. Danny despises him, claiming he is a vampire hunter, which he denies.

Hayden Szeto as Jonathan – A LARPer college student that Guillermo lured for the vampires to feast on. However, Colin Robinson beat them to it by draining his energy instead.

Danny Trejo as Danny – A Hispanic tattooed member of the council. He has an open dislike towards Wesley.

Taika Waititi, Jonathan Brugh, and Jemaine Clement reprise their roles as Viago von Dorna Schmarten Scheden Heimburg, Deacon Brucke, and Vladislav the Poker from the original film. Three vampires arrived from New Zealand to participate in the Vampiric Council.

Bobby Wilson as Marcus – The actual Native American member of the Werewolf Pack. He is Native American, and a werewolf but, as he explains, "Not a werewolf because" he is Native American. "It's not an ethnic thing."

Evan Rachel Wood as Evan the Immortal Princess of the Undead – A member of the Council who just goes by her first name.

Hannan Younis as Ange – An African American werewolf and part of Arjan's group. She undermines Arjan's rules and is openly hostile towards Nadja due to Nadja's insulting the werewolves by assuming they are all "Indian" (as in, Native Americans).

James Frain as the voice of Black Peter – A goat and witch's familiar

Mark Hamill as Jim the Vampire – A vampire who claims that Laszlo owes him rent money from the 1800s and demands retribution.

Greta Lee as Celeste – A familiar who pretends to be a vampire

Lucy Punch as Lilith – A witch and rival of Nadja

Craig Robinson as Claude – The leader of the Mosquito Collectors of the Tri-State Area, a secret team of amateur vampire hunters.

Julie Klausner and Cole Escola as The Gargoyles – A duo of gargoyles who gossip and give tips to The Guide.

Lauren Collins as Meg – A gym receptionist on whom Nandor has a crush.

Tyler Alvarez as Wes Blankenship – The leader of a group of rebellious young vampires that refuse to follow the council's orders.

Aida Turturro as Gail – Nandor's on-again, off-again werewolf-turned-vampire girlfriend.

Catherine Cohen as Sheila – The siren

Scott Bakula as himself

Cree Summer as Jan – A vampire scam artist who is head of the Post-Chiropteran Wellness Center cult

Donal Logue as a fictionalized vampire version of himself

Khandi Alexander as Contessa Carmilla De Mornay

David Cross as Dominykas the Dreadful

Affion Crockett as Richie Suck, superstar vampire rapper

Fred Armisen as Doctor DJ Tom Schmidt, Richie Suck's familiar who is manipulating him for financial gain.

Sal Vulcano as himself

Sklar Brothers as Toby and Bran

Al Roberts as Freddie, Guillermo's boyfriend

Sofia Coppola as herself

Thomas Mars as himself

Jim Jarmusch as himself

Michael McDonald as Gustave Leroy

Robert Smigel as Alexander, a man Nandor befriends at the gym

Hannibal Buress as a member of the energy vampire council

Aparna Nancherla as a member of the energy vampire council

Martha Kelly as the chair of the energy vampire council

Gregg Turkington as a member of the energy vampire council

Jo Firestone as a member of the energy vampire council

John Slattery as himself

Wayne Federman as a vampire urgent care doctor

Kerri Kenney-Silver as Helen "The Magic Woman" Johnson

Patton Oswalt as himself

Steve Coogan as Lord Roderick Cravensworth, Laszlo's father

Jon Glaser as a demon

Kevin Pollak as Cal Bodian, the lead actor of the TV series P.I. Undercover: New York

Zach Woods as Joel, an old office work friend of Colin Robinson

Alexander Skarsgård as a vampire

Critical response

All six seasons of What We Do in the Shadows received critical acclaim. On the review aggregator website Rotten Tomatoes, the overall series holds a 96% approval rating. On Metacritic, which uses a weighted average, the overall series has received a score of 83 out of 100.

The first season received positive reviews. On Rotten Tomatoes, the first season has an approval rating of 94%, based on 72 reviews, with an average rating of 7.8/10. The website's critical consensus reads, "Delightfully absurd and ridiculously fun, What We Do in the Shadows expands on the film's vampiric lore and finds fresh perspective in its charming, off-kilter cast to create a mockumentary series worth sinking your teeth into." On Metacritic, it has a weighted average score of 80 out of 100, based on 30 critics, indicating "generally favorable" reviews.

The second season also received positive reviews. On Rotten Tomatoes, the second season has an approval rating of 98%, based on 44 reviews, with an average rating of 8.3/10. The website's critical consensus reads, "Bat! What We Do In the Shadows loses no steam in a smashing second season that savvily expands its supernatural horizons while doubling down on the fast flying fun." On Metacritic, it has a weighted average score of 79 out of 100, based on 11 critics, indicating "generally favorable" reviews.

The third season was also praised. On Rotten Tomatoes, it has an approval rating of 100%, based on 28 reviews, with an average rating of 9/10. The website's critical consensus reads, "Carried on the wings of its cast's incredible chemistry and the strongest writing of the series so far, What We Do in the Shadows' third season is scary good." On Metacritic, the third season has an average score of 96 out of 100, based on 11 critics, indicating "universal acclaim".

The fourth season also received acclaim from critics. On Rotten Tomatoes, it has an approval rating of 100%, based on 29 reviews, with an average rating of 8.6/10. The website's critical consensus reads, "Aside from turning this demonic household into Three Vampires and a Baby, What We Do in the Shadows doubles down on what it does best without drastically changing the formula – and remains fang-tastic all the same." On Metacritic, the fourth season has an average score of 84 out of 100, based on eight critics, indicating "universal acclaim". However, some critics complained of the reductive treatment of Nandor's wife, Marwa, in season 4. Comic Book Resources complained of the show "stripping a woman of her identity – physically and mentally – for laughs" and The Mary Sue stated that "What We Do in the Shadows missed hard with its treatment of Marwa."

The fifth season also received positive reviews. On Rotten Tomatoes, it has an approval rating of 95%, based on 35 reviews, with an average rating of 7.65/10. The site's critical consensus reads, "Displaying a comedic longevity that'd make even a vampire blush, What We Do in the Shadows enters its fifth season showing no signs of getting long in the fang." On Metacritic, the fifth season has an average score of 85 out of 100, based on 11 critics, indicating "universal acclaim".

The sixth season also received positive reviews. On Rotten Tomatoes, it has an approval rating of 91%, based on 23 reviews, with an average rating of 7.8/10. The site's critical consensus reads, "What We Do in the Shadows wisely chooses to stick a stake in it before the Staten Island shenanigans become stale, preserving its integrity as one of television's best sitcoms." On Metacritic, the sixth season has an average score of 79 out of 100, based on 8 critics, indicating "generally favorable reviews".