diff --git a/src/cargo/util/toml/mod.rs b/src/cargo/util/toml/mod.rs
index aa083be3a29..85eb64ede96 100644
--- a/src/cargo/util/toml/mod.rs
+++ b/src/cargo/util/toml/mod.rs
@@ -458,10 +458,7 @@ impl ser::Serialize for ProfilePackageSpec {
     where
         S: ser::Serializer,
     {
-        match *self {
-            ProfilePackageSpec::Spec(ref spec) => spec.serialize(s),
-            ProfilePackageSpec::All => "*".serialize(s),
-        }
+        self.to_string().serialize(s)
     }
 }
 
@@ -481,6 +478,15 @@ impl<'de> de::Deserialize<'de> for ProfilePackageSpec {
     }
 }
 
+impl fmt::Display for ProfilePackageSpec {
+    fn fmt(&self, f: &mut fmt::Formatter<'_>) -> fmt::Result {
+        match self {
+            ProfilePackageSpec::Spec(spec) => spec.fmt(f),
+            ProfilePackageSpec::All => f.write_str("*"),
+        }
+    }
+}
+
 impl TomlProfile {
     pub fn validate(
         &self,
@@ -488,14 +494,17 @@ impl TomlProfile {
         features: &Features,
         warnings: &mut Vec<String>,
     ) -> CargoResult<()> {
+        self.validate_profile(name, features)?;
         if let Some(ref profile) = self.build_override {
             features.require(Feature::profile_overrides())?;
-            profile.validate_override("build-override", features)?;
+            profile.validate_override("build-override")?;
+            profile.validate_profile(&format!("{name}.build-override"), features)?;
         }
         if let Some(ref packages) = self.package {
             features.require(Feature::profile_overrides())?;
-            for profile in packages.values() {
-                profile.validate_override("package", features)?;
+            for (override_name, profile) in packages {
+                profile.validate_override("package")?;
+                profile.validate_profile(&format!("{name}.package.{override_name}"), features)?;
             }
         }
 
@@ -558,21 +567,6 @@ impl TomlProfile {
             }
         }
 
-        if self.rustflags.is_some() {
-            features.require(Feature::profile_rustflags())?;
-        }
-
-        if let Some(codegen_backend) = &self.codegen_backend {
-            features.require(Feature::codegen_backend())?;
-            if codegen_backend.contains(|c: char| !c.is_ascii_alphanumeric() && c != '_') {
-                bail!(
-                    "`profile.{}.codegen-backend` setting of `{}` is not a valid backend name.",
-                    name,
-                    codegen_backend,
-                );
-            }
-        }
-
         Ok(())
     }
 
@@ -655,7 +649,28 @@ impl TomlProfile {
         Ok(())
     }
 
-    fn validate_override(&self, which: &str, features: &Features) -> CargoResult<()> {
+    /// Validates a profile.
+    ///
+    /// This is a shallow check, which is reused for the profile itself and any overrides.
+    fn validate_profile(&self, name: &str, features: &Features) -> CargoResult<()> {
+        if let Some(codegen_backend) = &self.codegen_backend {
+            features.require(Feature::codegen_backend())?;
+            if codegen_backend.contains(|c: char| !c.is_ascii_alphanumeric() && c != '_') {
+                bail!(
+                    "`profile.{}.codegen-backend` setting of `{}` is not a valid backend name.",
+                    name,
+                    codegen_backend,
+                );
+            }
+        }
+        if self.rustflags.is_some() {
+            features.require(Feature::profile_rustflags())?;
+        }
+        Ok(())
+    }
+
+    /// Validation that is specific to an override.
+    fn validate_override(&self, which: &str) -> CargoResult<()> {
         if self.package.is_some() {
             bail!("package-specific profiles cannot be nested");
         }
@@ -671,9 +686,6 @@ impl TomlProfile {
         if self.rpath.is_some() {
             bail!("`rpath` may not be specified in a `{}` profile", which)
         }
-        if self.codegen_backend.is_some() {
-            features.require(Feature::codegen_backend())?;
-        }
         Ok(())
     }
 
diff --git a/tests/testsuite/profiles.rs b/tests/testsuite/profiles.rs
index 4cd09bfd51e..04531e68423 100644
--- a/tests/testsuite/profiles.rs
+++ b/tests/testsuite/profiles.rs
@@ -3,6 +3,7 @@
 use std::env;
 
 use cargo_test_support::project;
+use cargo_test_support::registry::Package;
 
 #[cargo_test]
 fn profile_overrides() {
@@ -663,6 +664,41 @@ fn rustflags_requires_cargo_feature() {
             "\
 [ERROR] failed to parse manifest at `[CWD]/Cargo.toml`
 
+Caused by:
+  feature `profile-rustflags` is required
+
+  The package requires the Cargo feature called `profile-rustflags`, but that feature is \
+  not stabilized in this version of Cargo (1.[..]).
+  Consider adding `cargo-features = [\"profile-rustflags\"]` to the top of Cargo.toml \
+  (above the [package] table) to tell Cargo you are opting in to use this unstable feature.
+  See https://doc.rust-lang.org/nightly/cargo/reference/unstable.html#profile-rustflags-option \
+  for more information about the status of this feature.
+",
+        )
+        .run();
+
+    Package::new("bar", "1.0.0").publish();
+    p.change_file(
+        "Cargo.toml",
+        r#"
+            [package]
+            name = "foo"
+            version = "0.0.1"
+
+            [dependencies]
+            bar = "1.0"
+
+            [profile.dev.package.bar]
+            rustflags = ["-C", "link-dead-code=yes"]
+        "#,
+    );
+    p.cargo("check")
+        .masquerade_as_nightly_cargo()
+        .with_status(101)
+        .with_stderr(
+            "\
+error: failed to parse manifest at `[ROOT]/foo/Cargo.toml`
+
 Caused by:
   feature `profile-rustflags` is required