The actor starred opposite Van Der Beek for the duration of the teen drama in one of the central relationships - that of Dawson and Joey.
Van Der Beek died on Wednesday aged 48 after suffering from bowel cancer.
In a handwritten letter, which she posted on Instagram, Holmes said: "James, Thank you.
"To share space with your imagination is sacred - breathing the same air in the land of make believe and trusting that each others' hearts are safe in their expression ...
"These are some of the memories, along with laughter, conversations about life, James Taylor songs - adventures of a unique youth ..."
"Bravery. Compassion. Selflessness. Strength. An appreciation for life and the action taken to live life with the integrity that life is art-creating a beautiful marriage, six loving children - the journey of a hero.
"I mourn this loss with a heart holding the reality of his absence and deep gratitude for his imprint on it."
Van Der Beek rose to fame playing Dawson Leery in the popular US teen drama Dawson's Creek, which ran for six seasons from 1998 until 2003.
He starred opposite Holmes, Joshua Jackson and Michelle Williams as the central quartet of hyper-articulate teens who were constantly embroiled in complex romantic entanglements.
Celebrity friends of Van Der Beek, including Zoe Saldana and Jon M Chu, are among those who have donated to help his family with medical expenses.
Busy Philipps, who played Audrey Liddell in Dawson's Creek, wrote on Instagram: "My heart is deeply hurting for all of us today.
"Every person who knew James and loved him, anyone who loved his work or had the pleasure of meeting him, all of his dear friends and community that surrounded him as he battled this illness, especially his parents and brother and sister.
"But I am profoundly heartbroken for his incredible wife Kimberly and their six magical children.
"James Van Der Beek was one in a billion and he will be forever missed."
His death comes just months after the show's cast reunited to help raise money for his cancer treatment.
Sentiments were echoed by Kerr Smith, who starred alongside Van Der Beek for five seasons as Jack McPhee.
"I'm so grateful for being able to call James a brother," he said on Instagram.
"I'll miss him deeply. Rest Easy."
In September, the Dawson's Creek reunion event was organised in support of the US actor and the charity F Cancer.
The night was attended by his former co-stars, including Williams, Holmes and Jackson.
Van Der Beek had planned to be there, but was too unwell.
His role was taken by Hamilton creator Lin-Manuel Miranda, who posted a picture of himself and Van Der Beek's family from the night on Instagram and said his "whole heart" was with them.
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