diff --git a/crates/ruff_server/src/session/settings.rs b/crates/ruff_server/src/session/settings.rs
index 610c6d5bea..0786d29be2 100644
--- a/crates/ruff_server/src/session/settings.rs
+++ b/crates/ruff_server/src/session/settings.rs
@@ -1,4 +1,4 @@
-use std::{ops::Deref, str::FromStr};
+use std::{ffi::OsString, ops::Deref, path::PathBuf, str::FromStr};
 
 use lsp_types::Url;
 use ruff_linter::{line_width::LineLength, RuleSelector};
@@ -31,6 +31,7 @@ pub(crate) struct ResolvedClientSettings {
 #[derive(Clone, Debug)]
 #[cfg_attr(test, derive(PartialEq, Eq))]
 pub(crate) struct ResolvedEditorSettings {
+    pub(super) configuration: Option<PathBuf>,
     pub(super) lint_preview: Option<bool>,
     pub(super) format_preview: Option<bool>,
     pub(super) select: Option<Vec<RuleSelector>>,
@@ -44,11 +45,10 @@ pub(crate) struct ResolvedEditorSettings {
 /// Determines how multiple conflicting configurations should be resolved - in this
 /// case, the configuration from the client settings and configuration from local
 /// `.toml` files (aka 'workspace' configuration).
-#[derive(Clone, Copy, Debug, Deserialize, Default)]
-#[cfg_attr(test, derive(PartialEq, Eq))]
+#[derive(Clone, Copy, Debug, Deserialize, Default, PartialEq, Eq)]
 #[serde(rename_all = "camelCase")]
 pub(crate) enum ConfigurationPreference {
-    /// Configuration set in the editor takes priority over workspace configuration set in `.toml` files.
+    /// Configuration set in the editor takes priority over configuration set in `.toml` files.
     #[default]
     EditorFirst,
     /// Configuration set in `.toml` files takes priority over configuration set in the editor.
@@ -62,6 +62,7 @@ pub(crate) enum ConfigurationPreference {
 #[cfg_attr(test, derive(PartialEq, Eq))]
 #[serde(rename_all = "camelCase")]
 pub(crate) struct ClientSettings {
+    configuration: Option<String>,
     fix_all: Option<bool>,
     organize_imports: Option<bool>,
     lint: Option<LintOptions>,
@@ -229,6 +230,12 @@ impl ResolvedClientSettings {
                 true,
             ),
             editor_settings: ResolvedEditorSettings {
+                configuration: Self::resolve_optional(all_settings, |settings| {
+                    settings
+                        .configuration
+                        .as_ref()
+                        .map(|config_path| OsString::from(config_path.clone()).into())
+                }),
                 lint_preview: Self::resolve_optional(all_settings, |settings| {
                     settings.lint.as_ref()?.preview
                 }),
@@ -357,6 +364,7 @@ mod tests {
         assert_debug_snapshot!(options, @r###"
         HasWorkspaces {
             global_settings: ClientSettings {
+                configuration: None,
                 fix_all: Some(
                     false,
                 ),
@@ -411,6 +419,7 @@ mod tests {
             workspace_settings: [
                 WorkspaceSettings {
                     settings: ClientSettings {
+                        configuration: None,
                         fix_all: Some(
                             true,
                         ),
@@ -469,6 +478,7 @@ mod tests {
                 },
                 WorkspaceSettings {
                     settings: ClientSettings {
+                        configuration: None,
                         fix_all: Some(
                             true,
                         ),
@@ -555,6 +565,7 @@ mod tests {
                 disable_rule_comment_enable: false,
                 fix_violation_enable: false,
                 editor_settings: ResolvedEditorSettings {
+                    configuration: None,
                     lint_preview: Some(true),
                     format_preview: None,
                     select: Some(vec![
@@ -584,6 +595,7 @@ mod tests {
                 disable_rule_comment_enable: true,
                 fix_violation_enable: false,
                 editor_settings: ResolvedEditorSettings {
+                    configuration: None,
                     lint_preview: Some(false),
                     format_preview: None,
                     select: Some(vec![
@@ -608,6 +620,7 @@ mod tests {
         GlobalOnly {
             settings: Some(
                 ClientSettings {
+                    configuration: None,
                     fix_all: Some(
                         false,
                     ),
@@ -671,6 +684,7 @@ mod tests {
                 disable_rule_comment_enable: false,
                 fix_violation_enable: true,
                 editor_settings: ResolvedEditorSettings {
+                    configuration: None,
                     lint_preview: None,
                     format_preview: None,
                     select: None,
diff --git a/crates/ruff_server/src/session/workspace/ruff_settings.rs b/crates/ruff_server/src/session/workspace/ruff_settings.rs
index c8da8f3de4..120713e069 100644
--- a/crates/ruff_server/src/session/workspace/ruff_settings.rs
+++ b/crates/ruff_server/src/session/workspace/ruff_settings.rs
@@ -110,6 +110,7 @@ impl<'a> ConfigurationTransformer for EditorConfigurationTransformer<'a> {
         filesystem_configuration: ruff_workspace::configuration::Configuration,
     ) -> ruff_workspace::configuration::Configuration {
         let ResolvedEditorSettings {
+            configuration,
             format_preview,
             lint_preview,
             select,
@@ -150,6 +151,19 @@ impl<'a> ConfigurationTransformer for EditorConfigurationTransformer<'a> {
             ..Default::default()
         };
 
+        // Merge in the editor-specified configuration file, if it exists
+        let editor_configuration = if let Some(config_file_path) = configuration {
+            match open_configuration_file(&config_file_path, project_root) {
+                Ok(config_from_file) => editor_configuration.combine(config_from_file),
+                Err(err) => {
+                    tracing::error!("Unable to find editor-specified configuration file {err}");
+                    editor_configuration
+                }
+            }
+        } else {
+            editor_configuration
+        };
+
         match configuration_preference {
             ConfigurationPreference::EditorFirst => {
                 editor_configuration.combine(filesystem_configuration)
@@ -161,3 +175,12 @@ impl<'a> ConfigurationTransformer for EditorConfigurationTransformer<'a> {
         }
     }
 }
+
+fn open_configuration_file(
+    config_path: &Path,
+    project_root: &Path,
+) -> crate::Result<Configuration> {
+    let options = ruff_workspace::pyproject::load_options(config_path)?;
+
+    Configuration::from_options(options, Some(config_path), project_root)
+}