To him, she was simply "mama".
Culkin joined O'Hara's Schitt's Creek co-stars Annie Murphy and Dan Levy on stage at Monday night's Emmy Awards for an emotional tribute to the revered comic actor, who died January 30 at age 71.
"She wasn't just a wife to Bo (Welch) and mother to Matthew and Luke," Culkin said.
"She was my mom. She was our mama, and by extension, she's all of our mama."
Culkin urged viewers to call their mothers and recalled how O'Hara continued to show up for him decades after they starred together in two Home Alone movies.
O'Hara played Kate McCallister, the frantic mother of Culkin's Kevin, in the 1990 original and its 1992 sequel, two holiday blockbusters that became perennial television favourites.
"This is the best that we can do for her tonight. We're showing up for her," he said.
"She may have forgotten me twice, but we will always remember her."
O'Hara died from a pulmonary embolism, with rectal cancer listed as the underlying cause.
Her career spanned five decades, from the Canadian sketch series SCTV to the Home Alone films, Christopher Guest's mockumentaries and her Emmy-winning performance as Moira Rose on Schitt's Creek.
The in-memoriam segment honoured O'Hara and other members of the television industry who died in the past year.
The montage also remembered entertainment icon Dolly Parton, actor and filmmaker Rob Reiner, actor Isiah Whitlock Jr and costume designer Bob Mackie, who was included despite dying earlier the same day as the ceremony.
Murphy, who played O'Hara's daughter, Alexis Rose, on Schitt's Creek, remembered her co-star's unmistakable laugh and the joy she brought to audiences.
"Catherine's laugh was a perpetual 'yes, and'," Murphy said.
"It challenged anyone who heard it to join in and be as delighted as she was, and she spread that delight everywhere."
Levy, who co-created Schitt's Creek and played O'Hara's on-screen son David Rose, said the greatest lesson he learned from her was to "always say yes", particularly to her creative instincts.
He also remembered O'Hara's generosity away from the set.
"Say yes to her dinner invites and her stories and her wisdom and her generosity," he said.
"Always say yes to any opportunity to revel in the presence of greatness."
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