diff --git a/src/cargo/util/context/mod.rs b/src/cargo/util/context/mod.rs
index f275c23877a..c4fa1a5947d 100644
--- a/src/cargo/util/context/mod.rs
+++ b/src/cargo/util/context/mod.rs
@@ -1035,6 +1035,11 @@ impl GlobalContext {
             self.cli_config = Some(cli_config.iter().map(|s| s.to_string()).collect());
             self.merge_cli_args()?;
         }
+
+        // Load the unstable flags from config file here first, as the config
+        // file itself may enable inclusion of other configs. In that case, we
+        // want to re-load configs with includes enabled:
+        self.load_unstable_flags_from_config()?;
         if self.unstable_flags.config_include {
             // If the config was already loaded (like when fetching the
             // `[alias]` table), it was loaded with includes disabled because
@@ -1091,8 +1096,6 @@ impl GlobalContext {
         let cli_target_dir = target_dir.as_ref().map(|dir| Filesystem::new(dir.clone()));
         self.target_dir = cli_target_dir;
 
-        self.load_unstable_flags_from_config()?;
-
         Ok(())
     }
 
diff --git a/tests/testsuite/config_include.rs b/tests/testsuite/config_include.rs
index d8f1dab972b..502ac7e919f 100644
--- a/tests/testsuite/config_include.rs
+++ b/tests/testsuite/config_include.rs
@@ -48,6 +48,171 @@ fn simple() {
     assert_eq!(gctx.get::<i32>("key3").unwrap(), 4);
 }
 
+#[cargo_test]
+fn enable_in_unstable_config() {
+    // config-include enabled in the unstable config table:
+    write_config_at(
+        ".cargo/config.toml",
+        "
+        include = 'other.toml'
+        key1 = 1
+        key2 = 2
+
+        [unstable]
+        config-include = true
+        ",
+    );
+    write_config_at(
+        ".cargo/other.toml",
+        "
+        key2 = 3
+        key3 = 4
+        ",
+    );
+    let gctx = GlobalContextBuilder::new()
+        .nightly_features_allowed(true)
+        .build();
+    assert_eq!(gctx.get::<i32>("key1").unwrap(), 1);
+    assert_eq!(gctx.get::<i32>("key2").unwrap(), 2);
+    assert_eq!(gctx.get::<i32>("key3").unwrap(), 4);
+}
+
+#[cargo_test]
+fn mix_of_hierarchy_and_include() {
+    write_config_at(
+        "foo/.cargo/config.toml",
+        "
+        include = 'other.toml'
+        key1 = 1
+
+        # also make sure unstable flags merge in the correct order
+        [unstable]
+        features = ['1']
+        ",
+    );
+    write_config_at(
+        "foo/.cargo/other.toml",
+        "
+        key1 = 2
+        key2 = 2
+
+        [unstable]
+        features = ['2']
+        ",
+    );
+    write_config_at(
+        ".cargo/config.toml",
+        "
+        include = 'other.toml'
+        key1 = 3
+        key2 = 3
+        key3 = 3
+
+        [unstable]
+        features = ['3']
+        ",
+    );
+    write_config_at(
+        ".cargo/other.toml",
+        "
+        key1 = 4
+        key2 = 4
+        key3 = 4
+        key4 = 4
+
+        [unstable]
+        features = ['4']
+        ",
+    );
+    let gctx = GlobalContextBuilder::new()
+        .unstable_flag("config-include")
+        .cwd("foo")
+        .nightly_features_allowed(true)
+        .build();
+    assert_eq!(gctx.get::<i32>("key1").unwrap(), 1);
+    assert_eq!(gctx.get::<i32>("key2").unwrap(), 2);
+    assert_eq!(gctx.get::<i32>("key3").unwrap(), 3);
+    assert_eq!(gctx.get::<i32>("key4").unwrap(), 4);
+    assert_eq!(
+        gctx.get::<Vec<String>>("unstable.features").unwrap(),
+        vec![
+            "4".to_string(),
+            "3".to_string(),
+            "2".to_string(),
+            "1".to_string()
+        ]
+    );
+}
+
+#[cargo_test]
+fn mix_of_hierarchy_and_include_with_enable_in_unstable_config() {
+    // `mix_of_hierarchy_and_include`, but with the config-include
+    // feature itself enabled in the unstable config table:
+    write_config_at(
+        "foo/.cargo/config.toml",
+        "
+        include = 'other.toml'
+        key1 = 1
+
+        # also make sure unstable flags merge in the correct order
+        [unstable]
+        features = ['1']
+        config-include = true
+        ",
+    );
+    write_config_at(
+        "foo/.cargo/other.toml",
+        "
+        key1 = 2
+        key2 = 2
+
+        [unstable]
+        features = ['2']
+        ",
+    );
+    write_config_at(
+        ".cargo/config.toml",
+        "
+        include = 'other.toml'
+        key1 = 3
+        key2 = 3
+        key3 = 3
+
+        [unstable]
+        features = ['3']
+        ",
+    );
+    write_config_at(
+        ".cargo/other.toml",
+        "
+        key1 = 4
+        key2 = 4
+        key3 = 4
+        key4 = 4
+
+        [unstable]
+        features = ['4']
+        ",
+    );
+    let gctx = GlobalContextBuilder::new()
+        .cwd("foo")
+        .nightly_features_allowed(true)
+        .build();
+    assert_eq!(gctx.get::<i32>("key1").unwrap(), 1);
+    assert_eq!(gctx.get::<i32>("key2").unwrap(), 2);
+    assert_eq!(gctx.get::<i32>("key3").unwrap(), 3);
+    assert_eq!(gctx.get::<i32>("key4").unwrap(), 4);
+    assert_eq!(
+        gctx.get::<Vec<String>>("unstable.features").unwrap(),
+        vec![
+            "4".to_string(),
+            "3".to_string(),
+            "2".to_string(),
+            "1".to_string()
+        ]
+    );
+}
+
 #[cargo_test]
 fn works_with_cli() {
     write_config_at(