diff --git a/CHANGELOG.md b/CHANGELOG.md
index 4c161d69..08faff05 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -34,6 +34,8 @@
 
 - Air no longer emits colored output when stderr is not a terminal, such as when stderr is redirected to a file.
 
+- `#line` directives are no longer indented, since R only reads them as directives at the start of a line (#425).
+
 # 0.12.0
 
 - New `--no-configuration` flag to format with Air's built-in defaults without loading a project or user configuration file (#479, @LeonidasZhak).
diff --git a/crates/air_r_formatter/src/comments.rs b/crates/air_r_formatter/src/comments.rs
index 60fbd62f..8bdef9a2 100644
--- a/crates/air_r_formatter/src/comments.rs
+++ b/crates/air_r_formatter/src/comments.rs
@@ -21,6 +21,7 @@ use biome_formatter::comments::CommentTextPosition;
 use biome_formatter::comments::Comments;
 use biome_formatter::comments::DecoratedComment;
 use biome_formatter::comments::SourceComment;
+use biome_formatter::format_args;
 use biome_formatter::write;
 use biome_rowan::AstNode;
 use biome_rowan::Direction;
@@ -41,12 +42,41 @@ impl FormatRule<SourceComment<RLanguage>> for FormatRLeadingComment {
         comment: &SourceComment<RLanguage>,
         f: &mut Formatter<Self::Context>,
     ) -> FormatResult<()> {
+        // A `#line` directive is only read as one when it is the first thing on
+        // its line, so it is written at the start of the line whatever the
+        // indentation around it. The line break inside the dedent doesn't add a
+        // line, it only resets the indentation of the line the comment starts.
+        if is_line_directive(comment) {
+            return write!(
+                f,
+                [dedent_to_root(&format_args![
+                    hard_line_break(),
+                    comment.piece().as_piece()
+                ])]
+            );
+        }
+
         // It seems like this is only worth customizing for multi-line comments
         // that need to be aligned together
         write!(f, [comment.piece().as_piece()])
     }
 }
 
+/// Whether the comment is a `#line` directive, which maps source references in
+/// generated code back to another file. R reads `#line` followed by a line
+/// number as one, but only at the start of a line.
+fn is_line_directive(comment: &SourceComment<RLanguage>) -> bool {
+    comment.lines_before() > 0
+        && comment
+            .piece()
+            .text()
+            .strip_prefix("#line")
+            .is_some_and(|rest| {
+                rest.trim_start_matches([' ', '\t'])
+                    .starts_with(|c: char| c.is_ascii_digit())
+            })
+}
+
 #[derive(Eq, PartialEq, Copy, Clone, Debug, Default)]
 pub struct RCommentStyle;
 
diff --git a/crates/air_r_formatter/tests/specs/r/comment_line_directive.R b/crates/air_r_formatter/tests/specs/r/comment_line_directive.R
new file mode 100644
index 00000000..413fb815
--- /dev/null
+++ b/crates/air_r_formatter/tests/specs/r/comment_line_directive.R
@@ -0,0 +1,28 @@
+#line 1 "top.R"
+x <- 1
+
+{
+#line 1 "file1.R"
+  withAutoprint({ show.srcref() })
+}
+
+f <- function() {
+  x
+#line 10 "gen.R"
+  y
+}
+
+fn(
+  a,
+#line 20 "gen.R"
+  b
+)
+
+{
+  # Comments that only look like one stay indented
+#lines of text
+#line up the columns
+  z
+}
+
+x #line 30 "gen.R"
diff --git a/crates/air_r_formatter/tests/specs/r/comment_line_directive.R.snap b/crates/air_r_formatter/tests/specs/r/comment_line_directive.R.snap
new file mode 100644
index 00000000..4a504543
--- /dev/null
+++ b/crates/air_r_formatter/tests/specs/r/comment_line_directive.R.snap
@@ -0,0 +1,87 @@
+---
+source: crates/air_formatter_test/src/snapshot_builder.rs
+info: r/comment_line_directive.R
+---
+# Input
+
+```R
+#line 1 "top.R"
+x <- 1
+
+{
+#line 1 "file1.R"
+  withAutoprint({ show.srcref() })
+}
+
+f <- function() {
+  x
+#line 10 "gen.R"
+  y
+}
+
+fn(
+  a,
+#line 20 "gen.R"
+  b
+)
+
+{
+  # Comments that only look like one stay indented
+#lines of text
+#line up the columns
+  z
+}
+
+x #line 30 "gen.R"
+
+```
+
+
+=============================
+
+# Outputs
+
+## Output 1
+
+-----
+Indent style: Space
+Indent width: 2
+Line ending: LF
+Line width: 80
+Persistent line breaks: Respect
+Assignment style: Arrow
+Table: fcase, rowwiseDT, tribble
+-----
+
+```R
+#line 1 "top.R"
+x <- 1
+
+{
+#line 1 "file1.R"
+  withAutoprint({
+    show.srcref()
+  })
+}
+
+f <- function() {
+  x
+#line 10 "gen.R"
+  y
+}
+
+fn(
+  a,
+#line 20 "gen.R"
+  b
+)
+
+{
+  # Comments that only look like one stay indented
+  #lines of text
+  #line up the columns
+  z
+}
+
+x #line 30 "gen.R"
+```