diff --git a/crates/red_knot/src/main.rs b/crates/red_knot/src/main.rs
index 812d994d3a152..0a7529a04546b 100644
--- a/crates/red_knot/src/main.rs
+++ b/crates/red_knot/src/main.rs
@@ -104,7 +104,7 @@ pub fn main() -> anyhow::Result<()> {
             extra_paths,
             workspace_root: workspace_metadata.root().to_path_buf(),
             custom_typeshed: custom_typeshed_dir,
-            site_packages: None,
+            site_packages: vec![],
         },
     };
 
diff --git a/crates/red_knot/tests/file_watching.rs b/crates/red_knot/tests/file_watching.rs
index c74ab4efdb287..dad017280ff2c 100644
--- a/crates/red_knot/tests/file_watching.rs
+++ b/crates/red_knot/tests/file_watching.rs
@@ -181,7 +181,7 @@ where
         extra_paths: vec![],
         workspace_root: workspace_path.to_path_buf(),
         custom_typeshed: None,
-        site_packages: None,
+        site_packages: vec![],
     })
 }
 
@@ -697,7 +697,7 @@ fn search_path() -> anyhow::Result<()> {
                 extra_paths: vec![],
                 workspace_root: workspace_path.to_path_buf(),
                 custom_typeshed: None,
-                site_packages: Some(root_path.join("site_packages")),
+                site_packages: vec![root_path.join("site_packages")],
             }
         })?;
 
@@ -734,7 +734,7 @@ fn add_search_path() -> anyhow::Result<()> {
 
     // Register site-packages as a search path.
     case.update_search_path_settings(|settings| SearchPathSettings {
-        site_packages: Some(site_packages.clone()),
+        site_packages: vec![site_packages.clone()],
         ..settings.clone()
     });
 
@@ -757,14 +757,14 @@ fn remove_search_path() -> anyhow::Result<()> {
                 extra_paths: vec![],
                 workspace_root: workspace_path.to_path_buf(),
                 custom_typeshed: None,
-                site_packages: Some(root_path.join("site_packages")),
+                site_packages: vec![root_path.join("site_packages")],
             }
         })?;
 
     // Remove site packages from the search path settings.
     let site_packages = case.root_path().join("site_packages");
     case.update_search_path_settings(|settings| SearchPathSettings {
-        site_packages: None,
+        site_packages: vec![],
         ..settings.clone()
     });
 
@@ -1175,7 +1175,7 @@ mod unix {
                 extra_paths: vec![],
                 workspace_root: workspace.to_path_buf(),
                 custom_typeshed: None,
-                site_packages: Some(workspace.join(".venv/lib/python3.12/site-packages")),
+                site_packages: vec![workspace.join(".venv/lib/python3.12/site-packages")],
             },
         )?;
 
diff --git a/crates/red_knot_module_resolver/src/resolver.rs b/crates/red_knot_module_resolver/src/resolver.rs
index a1c5f46a6bc8d..b66d706566abe 100644
--- a/crates/red_knot_module_resolver/src/resolver.rs
+++ b/crates/red_knot_module_resolver/src/resolver.rs
@@ -160,11 +160,18 @@ fn try_resolve_module_resolution_settings(
         SearchPath::vendored_stdlib()
     });
 
-    if let Some(site_packages) = site_packages {
-        files.try_add_root(db.upcast(), site_packages, FileRootKind::LibrarySearchPath);
+    for site_packages_dir in site_packages {
+        files.try_add_root(
+            db.upcast(),
+            site_packages_dir,
+            FileRootKind::LibrarySearchPath,
+        );
 
-        static_search_paths.push(SearchPath::site_packages(system, site_packages.clone())?);
-    };
+        static_search_paths.push(SearchPath::site_packages(
+            system,
+            site_packages_dir.clone(),
+        )?);
+    }
 
     // TODO vendor typeshed's third-party stubs as well as the stdlib and fallback to them as a final step
 
@@ -1180,7 +1187,7 @@ mod tests {
             extra_paths: vec![],
             workspace_root: src.clone(),
             custom_typeshed: Some(custom_typeshed.clone()),
-            site_packages: Some(site_packages.clone()),
+            site_packages: vec![site_packages],
         };
 
         Program::new(&db, TargetVersion::Py38, search_paths);
diff --git a/crates/red_knot_module_resolver/src/testing.rs b/crates/red_knot_module_resolver/src/testing.rs
index 3a9e3e8d4f87e..51f4b30f640d2 100644
--- a/crates/red_knot_module_resolver/src/testing.rs
+++ b/crates/red_knot_module_resolver/src/testing.rs
@@ -12,6 +12,9 @@ pub(crate) struct TestCase<T> {
     pub(crate) db: TestDb,
     pub(crate) src: SystemPathBuf,
     pub(crate) stdlib: T,
+    // Most test cases only ever need a single `site-packages` directory,
+    // so this is a single directory instead of a `Vec` of directories,
+    // like it is in `ruff_db::Program`.
     pub(crate) site_packages: SystemPathBuf,
     pub(crate) target_version: TargetVersion,
 }
@@ -223,7 +226,7 @@ impl TestCaseBuilder<MockedTypeshed> {
                 extra_paths: vec![],
                 workspace_root: src.clone(),
                 custom_typeshed: Some(typeshed.clone()),
-                site_packages: Some(site_packages.clone()),
+                site_packages: vec![site_packages.clone()],
             },
         );
 
@@ -276,7 +279,7 @@ impl TestCaseBuilder<VendoredTypeshed> {
                 extra_paths: vec![],
                 workspace_root: src.clone(),
                 custom_typeshed: None,
-                site_packages: Some(site_packages.clone()),
+                site_packages: vec![site_packages.clone()],
             },
         );
 
diff --git a/crates/red_knot_python_semantic/src/semantic_model.rs b/crates/red_knot_python_semantic/src/semantic_model.rs
index aa5702170cd7a..d2c479cb47b70 100644
--- a/crates/red_knot_python_semantic/src/semantic_model.rs
+++ b/crates/red_knot_python_semantic/src/semantic_model.rs
@@ -179,7 +179,7 @@ mod tests {
             SearchPathSettings {
                 extra_paths: vec![],
                 workspace_root: SystemPathBuf::from("/src"),
-                site_packages: None,
+                site_packages: vec![],
                 custom_typeshed: None,
             },
         );
diff --git a/crates/red_knot_python_semantic/src/types/infer.rs b/crates/red_knot_python_semantic/src/types/infer.rs
index f8cd746401e3e..c28fccc764a2d 100644
--- a/crates/red_knot_python_semantic/src/types/infer.rs
+++ b/crates/red_knot_python_semantic/src/types/infer.rs
@@ -1515,7 +1515,7 @@ mod tests {
             SearchPathSettings {
                 extra_paths: Vec::new(),
                 workspace_root: SystemPathBuf::from("/src"),
-                site_packages: None,
+                site_packages: vec![],
                 custom_typeshed: None,
             },
         );
@@ -1532,7 +1532,7 @@ mod tests {
             SearchPathSettings {
                 extra_paths: Vec::new(),
                 workspace_root: SystemPathBuf::from("/src"),
-                site_packages: None,
+                site_packages: vec![],
                 custom_typeshed: Some(SystemPathBuf::from(typeshed)),
             },
         );
diff --git a/crates/red_knot_workspace/src/lint.rs b/crates/red_knot_workspace/src/lint.rs
index 27114bf251427..20eac583ab14d 100644
--- a/crates/red_knot_workspace/src/lint.rs
+++ b/crates/red_knot_workspace/src/lint.rs
@@ -326,7 +326,7 @@ mod tests {
             SearchPathSettings {
                 extra_paths: Vec::new(),
                 workspace_root,
-                site_packages: None,
+                site_packages: vec![],
                 custom_typeshed: None,
             },
         );
diff --git a/crates/red_knot_workspace/tests/check.rs b/crates/red_knot_workspace/tests/check.rs
index a2d0f99207f02..ba92cc525bde8 100644
--- a/crates/red_knot_workspace/tests/check.rs
+++ b/crates/red_knot_workspace/tests/check.rs
@@ -14,7 +14,7 @@ fn setup_db(workspace_root: SystemPathBuf) -> anyhow::Result<RootDatabase> {
         extra_paths: vec![],
         workspace_root,
         custom_typeshed: None,
-        site_packages: None,
+        site_packages: vec![],
     };
     let settings = ProgramSettings {
         target_version: TargetVersion::default(),
diff --git a/crates/ruff_benchmark/benches/red_knot.rs b/crates/ruff_benchmark/benches/red_knot.rs
index 079bd17200814..cc307d5c01b2d 100644
--- a/crates/ruff_benchmark/benches/red_knot.rs
+++ b/crates/ruff_benchmark/benches/red_knot.rs
@@ -74,7 +74,7 @@ fn setup_case() -> Case {
         search_paths: SearchPathSettings {
             extra_paths: vec![],
             workspace_root: workspace_root.to_path_buf(),
-            site_packages: None,
+            site_packages: vec![],
             custom_typeshed: None,
         },
     };
diff --git a/crates/ruff_db/src/program.rs b/crates/ruff_db/src/program.rs
index c5cdc30de64fd..78f3fc5a3b259 100644
--- a/crates/ruff_db/src/program.rs
+++ b/crates/ruff_db/src/program.rs
@@ -81,5 +81,5 @@ pub struct SearchPathSettings {
     pub custom_typeshed: Option<SystemPathBuf>,
 
     /// The path to the user's `site-packages` directory, where third-party packages from ``PyPI`` are installed.
-    pub site_packages: Option<SystemPathBuf>,
+    pub site_packages: Vec<SystemPathBuf>,
 }