diff --git a/src/content-linter/scripts/lint-content.js b/src/content-linter/scripts/lint-content.js
index 3c5342a4be2d..679a126875da 100755
--- a/src/content-linter/scripts/lint-content.js
+++ b/src/content-linter/scripts/lint-content.js
@@ -551,7 +551,8 @@ function getMarkdownLintConfig(errorsOnly, runRules) {
       continue
     }
 
-    if (runRules && !runRules.includes(ruleName)) continue
+    // Check if the rule should be included based on user-specified rules
+    if (runRules && !shouldIncludeRule(ruleName, runRules)) continue
 
     // Skip british-english-quotes rule in CI/PRs (only run in pre-commit)
     if (ruleName === 'british-english-quotes' && !isPrecommit) continue
@@ -638,6 +639,29 @@ function getCustomRule(ruleName) {
   return rule
 }
 
+// Check if a rule should be included based on user-specified rules
+// Handles both short names (e.g., GHD053, MD001) and long names (e.g., header-content-requirement, heading-increment)
+export function shouldIncludeRule(ruleName, runRules) {
+  // First check if the rule name itself is in the list
+  if (runRules.includes(ruleName)) {
+    return true
+  }
+
+  // For custom rules, check if any of the rule's names (short or long) are in the runRules list
+  const customRule = customRules.find((rule) => rule.names.includes(ruleName))
+  if (customRule) {
+    return customRule.names.some((name) => runRules.includes(name))
+  }
+
+  // For built-in markdownlint rules, check if any of the rule's names are in the runRules list
+  const builtinRule = allRules.find((rule) => rule.names.includes(ruleName))
+  if (builtinRule) {
+    return builtinRule.names.some((name) => runRules.includes(name))
+  }
+
+  return false
+}
+
 /*
   The severity of the search-replace custom rule is embedded in
   each individual search rule. This function returns the severity
@@ -681,9 +705,7 @@ function isOptionsValid() {
   }
 
   // rules should only contain existing, correctly spelled rules
-  const allRulesList = Object.values(allRules)
-    .map((rule) => rule.names)
-    .flat()
+  const allRulesList = [...allRules.map((rule) => rule.names).flat(), ...Object.keys(allConfig)]
   const rules = program.opts().rules || []
   for (const rule of rules) {
     if (!allRulesList.includes(rule)) {
diff --git a/src/content-linter/tests/unit/rule-filtering.js b/src/content-linter/tests/unit/rule-filtering.js
new file mode 100644
index 000000000000..4ee5a27020bf
--- /dev/null
+++ b/src/content-linter/tests/unit/rule-filtering.js
@@ -0,0 +1,62 @@
+import { describe, test, expect, vi } from 'vitest'
+import { shouldIncludeRule } from '../../scripts/lint-content.js'
+
+// Mock the get-rules module to provide test data for rule definitions
+vi.mock('../../lib/helpers/get-rules', () => ({
+  allRules: [
+    {
+      names: ['MD001', 'heading-increment'],
+      description: 'Heading levels should only increment by one level at a time',
+    },
+    {
+      names: ['MD002', 'first-heading-h1'],
+      description: 'First heading should be a top level heading',
+    },
+  ],
+  customRules: [
+    {
+      names: ['GHD053', 'header-content-requirement'],
+      description: 'Headers must have content below them',
+    },
+    {
+      names: ['GHD030', 'code-fence-line-length'],
+      description: 'Code fence content should not exceed line length limit',
+    },
+  ],
+  allConfig: {},
+}))
+
+describe('shouldIncludeRule', () => {
+  test('includes rule by long name', () => {
+    expect(shouldIncludeRule('heading-increment', ['heading-increment'])).toBe(true)
+    expect(shouldIncludeRule('header-content-requirement', ['header-content-requirement'])).toBe(
+      true,
+    )
+  })
+
+  test('includes built-in rule by short code', () => {
+    expect(shouldIncludeRule('heading-increment', ['MD001'])).toBe(true)
+    expect(shouldIncludeRule('first-heading-h1', ['MD002'])).toBe(true)
+  })
+
+  test('includes custom rule by short code', () => {
+    expect(shouldIncludeRule('header-content-requirement', ['GHD053'])).toBe(true)
+    expect(shouldIncludeRule('code-fence-line-length', ['GHD030'])).toBe(true)
+  })
+
+  test('excludes rule not in list', () => {
+    expect(shouldIncludeRule('heading-increment', ['MD002'])).toBe(false)
+    expect(shouldIncludeRule('header-content-requirement', ['GHD030'])).toBe(false)
+  })
+
+  test('handles multiple rules', () => {
+    const runRules = ['MD001', 'GHD053', 'some-other-rule']
+    expect(shouldIncludeRule('heading-increment', runRules)).toBe(true)
+    expect(shouldIncludeRule('header-content-requirement', runRules)).toBe(true)
+    expect(shouldIncludeRule('first-heading-h1', runRules)).toBe(false)
+  })
+
+  test('handles unknown rules gracefully', () => {
+    expect(shouldIncludeRule('non-existent-rule', ['MD001'])).toBe(false)
+  })
+})