diff --git a/man/man1/fzf.1 b/man/man1/fzf.1
index a07222e1..c5f13622 100644
--- a/man/man1/fzf.1
+++ b/man/man1/fzf.1
@@ -1001,7 +1001,8 @@ The first N lines of the input are treated as the sticky header. When
 lines that follow.
 .TP
 .B "\-\-header\-first"
-Print header before the prompt line
+Print header before the prompt line. When both normal header and header lines
+(\fB\-\-header\-lines\fR) are present, this applies only to the normal header.
 .TP
 .BI "\-\-header\-border" [=STYLE]
 Draw border around the header section
diff --git a/src/options.go b/src/options.go
index 3def3395..142179e5 100644
--- a/src/options.go
+++ b/src/options.go
@@ -3218,15 +3218,6 @@ func postProcessOptions(opts *Options) error {
 
 	if opts.HeaderLinesShape == tui.BorderNone {
 		opts.HeaderLinesShape = tui.BorderPhantom
-	} else if opts.HeaderLinesShape == tui.BorderUndefined {
-		// In reverse-list layout, header lines should be at the top, while
-		// ordinary header should be at the bottom. So let's use a separate
-		// window for the header lines.
-		if opts.Layout == layoutReverseList {
-			opts.HeaderLinesShape = tui.BorderPhantom
-		} else {
-			opts.HeaderLinesShape = tui.BorderNone
-		}
 	}
 
 	if opts.Pointer == nil {
diff --git a/src/terminal.go b/src/terminal.go
index 8ffe9cef..a89551da 100644
--- a/src/terminal.go
+++ b/src/terminal.go
@@ -1203,8 +1203,8 @@ func (t *Terminal) extraLines() int {
 			extra += borderLines(t.headerBorderShape)
 		}
 		extra += len(t.header0)
-		if t.hasHeaderLinesWindow() {
-			extra += borderLines(t.headerLinesShape)
+		if w, shape := t.determineHeaderLinesShape(); w {
+			extra += borderLines(shape)
 		}
 		extra += t.headerLines
 	}
@@ -1770,7 +1770,46 @@ func (t *Terminal) hasHeaderWindow() bool {
 }
 
 func (t *Terminal) hasHeaderLinesWindow() bool {
-	return t.headerVisible && t.headerLines > 0 && t.headerLinesShape.Visible()
+	w, _ := t.determineHeaderLinesShape()
+	return w
+}
+
+func (t *Terminal) determineHeaderLinesShape() (bool, tui.BorderShape) {
+	if !t.headerVisible || t.headerLines == 0 {
+		return false, tui.BorderNone
+	}
+
+	// --header-lines-border is set
+	if t.headerLinesShape != tui.BorderUndefined {
+		return true, t.headerLinesShape
+	}
+
+	// --header-lines-border is not set, determine if we should use
+	// the style of --header-border
+	shape := tui.BorderNone
+	if len(t.header0) == 0 {
+		shape = t.headerBorderShape
+	}
+	if shape == tui.BorderNone {
+		shape = tui.BorderPhantom
+	}
+
+	// --layout reverse-list is set
+	if t.layout == layoutReverseList {
+		return true, shape
+	}
+
+	// Use header window instead
+	if len(t.header0) == 0 {
+		return false, t.headerBorderShape
+	}
+
+	// We have both types of headers, and we want to separate the two
+	if t.headerFirst {
+		return true, shape
+	}
+
+	return false, tui.BorderNone
 }
 
 func (t *Terminal) resizeWindows(forcePreview bool, redrawBorder bool) {
@@ -1853,7 +1892,7 @@ func (t *Terminal) resizeWindows(forcePreview bool, redrawBorder bool) {
 	shift := 0
 	shrink := 0
 	hasHeaderWindow := t.hasHeaderWindow()
-	hasHeaderLinesWindow := t.hasHeaderLinesWindow()
+	hasHeaderLinesWindow, headerLinesShape := t.determineHeaderLinesShape()
 	hasInputWindow := !t.inputless && (t.inputBorderShape.Visible() || hasHeaderWindow || hasHeaderLinesWindow)
 	if hasInputWindow {
 		inputWindowHeight := 2
@@ -1889,7 +1928,7 @@ func (t *Terminal) resizeWindows(forcePreview bool, redrawBorder bool) {
 
 	headerLinesHeight := 0
 	if hasHeaderLinesWindow {
-		headerLinesHeight = util.Min(availableLines, borderLines(t.headerLinesShape)+t.headerLines)
+		headerLinesHeight = util.Min(availableLines, borderLines(headerLinesShape)+t.headerLines)
 		if t.layout != layoutDefault {
 			shift += headerLinesHeight
 			shrink += headerLinesHeight
@@ -2147,23 +2186,33 @@ func (t *Terminal) resizeWindows(forcePreview bool, redrawBorder bool) {
 	if t.wborder == nil {
 		w = t.window
 	}
+
 	if hasInputWindow {
 		var btop int
-		if hasHeaderWindow && t.headerFirst {
-			if t.layout == layoutReverse {
-				btop = w.Top() - inputBorderHeight - headerLinesHeight
-			} else if t.layout == layoutReverseList {
+		if (hasHeaderWindow || hasHeaderLinesWindow) && t.headerFirst {
+			switch t.layout {
+			case layoutDefault:
+				btop = w.Top() + w.Height()
+				// If both headers are present, the header lines are displayed with the list
+				if hasHeaderWindow && hasHeaderLinesWindow {
+					btop += headerLinesHeight
+				}
+			case layoutReverse:
+				btop = w.Top() - inputBorderHeight
+				if hasHeaderWindow && hasHeaderLinesWindow {
+					btop -= headerLinesHeight
+				}
+			case layoutReverseList:
 				btop = w.Top() + w.Height()
-			} else {
-				btop = w.Top() + w.Height() + headerLinesHeight
 			}
 		} else {
-			if t.layout == layoutReverse {
-				btop = w.Top() - shrink
-			} else if t.layout == layoutReverseList {
-				btop = w.Top() + w.Height() + headerBorderHeight
-			} else {
+			switch t.layout {
+			case layoutDefault:
 				btop = w.Top() + w.Height() + headerBorderHeight + headerLinesHeight
+			case layoutReverse:
+				btop = w.Top() - shrink
+			case layoutReverseList:
+				btop = w.Top() + w.Height() + headerBorderHeight
 			}
 		}
 		shift := 0
@@ -2215,17 +2264,34 @@ func (t *Terminal) resizeWindows(forcePreview bool, redrawBorder bool) {
 	// Set up header lines border
 	if hasHeaderLinesWindow {
 		var btop int
-		if t.layout != layoutDefault {
-			btop = w.Top() - headerLinesHeight
+		// NOTE: We still have to handle --header-first here in case
+		// --header-lines-border is set. Can't we just use header window instead
+		// with the style? So we can display header label.
+		//   fzf --header-lines 3 --header-label hello --header-border
+		//   fzf --header-lines 3 --header-label hello --header-lines-border
+		headerFirst := t.headerFirst && len(t.header0) == 0
+
+		if headerFirst {
+			if t.layout == layoutDefault {
+				btop = w.Top() + w.Height() + inputBorderHeight
+			} else if t.layout == layoutReverse {
+				btop = w.Top() - headerLinesHeight - inputBorderHeight
+			} else {
+				btop = w.Top() - headerLinesHeight
+			}
 		} else {
-			btop = w.Top() + w.Height()
+			if t.layout != layoutDefault {
+				btop = w.Top() - headerLinesHeight
+			} else {
+				btop = w.Top() + w.Height()
+			}
 		}
 		t.headerLinesBorder = t.tui.NewWindow(
 			btop,
 			w.Left(),
 			w.Width(),
-			headerLinesHeight, tui.WindowHeader, tui.MakeBorderStyle(t.headerLinesShape, t.unicode), true)
-		t.headerLinesWindow = createInnerWindow(t.headerLinesBorder, t.headerLinesShape, tui.WindowHeader, 0)
+			headerLinesHeight, tui.WindowHeader, tui.MakeBorderStyle(headerLinesShape, t.unicode), true)
+		t.headerLinesWindow = createInnerWindow(t.headerLinesBorder, headerLinesShape, tui.WindowHeader, 0)
 	}
 
 	// Print border label
@@ -2621,12 +2687,14 @@ func (t *Terminal) resizeIfNeeded() bool {
 	// Check if the header borders are used and header has changed
 	allHeaderLines := t.visibleHeaderLines()
 	primaryHeaderLines := allHeaderLines
-	if t.headerLinesShape.Visible() {
+	if t.hasHeaderLinesWindow() {
 		primaryHeaderLines -= t.headerLines
 	}
-	if (t.headerBorderShape.Visible() || t.headerLinesShape.Visible()) &&
+	needHeaderLinesWindow := t.hasHeaderLinesWindow()
+	if (t.headerBorderShape.Visible() || t.hasHeaderLinesWindow()) &&
 		(t.headerWindow == nil && primaryHeaderLines > 0 || t.headerWindow != nil && primaryHeaderLines != t.headerWindow.Height()) ||
-		t.headerLinesShape.Visible() && (t.headerLinesWindow == nil && t.headerLines > 0 || t.headerLinesWindow != nil && t.headerLines != t.headerLinesWindow.Height()) {
+		needHeaderLinesWindow && (t.headerLinesWindow == nil || t.headerLinesWindow != nil && t.headerLines != t.headerLinesWindow.Height()) ||
+		!needHeaderLinesWindow && t.headerLinesWindow != nil {
 		t.printAll()
 		return true
 	}
@@ -2640,14 +2708,14 @@ func (t *Terminal) printHeader() {
 
 	t.withWindow(t.headerWindow, func() {
 		var lines []string
-		if !t.headerLinesShape.Visible() {
+		if !t.hasHeaderLinesWindow() {
 			lines = t.header
 		}
 		t.printHeaderImpl(t.headerWindow, t.headerBorderShape, t.header0, lines)
 	})
-	if t.headerLinesShape.Visible() {
+	if w, shape := t.determineHeaderLinesShape(); w {
 		t.withWindow(t.headerLinesWindow, func() {
-			t.printHeaderImpl(t.headerLinesWindow, t.headerLinesShape, nil, t.header)
+			t.printHeaderImpl(t.headerLinesWindow, shape, nil, t.header)
 		})
 	}
 }
@@ -5863,7 +5931,8 @@ func (t *Terminal) Loop() error {
 				}
 
 				if clicked && t.headerVisible && t.headerLinesWindow != nil && t.headerLinesWindow.Enclose(my, mx) {
-					mx -= t.headerLinesWindow.Left() + t.headerIndent(t.headerLinesShape)
+					_, shape := t.determineHeaderLinesShape()
+					mx -= t.headerLinesWindow.Left() + t.headerIndent(shape)
 					my -= t.headerLinesWindow.Top()
 					if mx < 0 {
 						break
diff --git a/test/test_layout.rb b/test/test_layout.rb
index 2d30c87a..152abb8c 100644
--- a/test/test_layout.rb
+++ b/test/test_layout.rb
@@ -39,11 +39,11 @@ class TestLayout < TestInteractive
     tmux.send_keys "seq 1000 | #{FZF} --header foobar --header-lines 3 --header-first", :Enter
     block = <<~OUTPUT
       > 4
-        997/997
-      >
         3
         2
         1
+        997/997
+      >
         foobar
     OUTPUT
     tmux.until { assert_block(block, it) }
@@ -53,10 +53,10 @@ class TestLayout < TestInteractive
     tmux.send_keys "seq 1000 | #{FZF} --header foobar --header-lines 3 --header-first --reverse --inline-info", :Enter
     block = <<~OUTPUT
         foobar
+      >   < 997/997
         1
         2
         3
-      >   < 997/997
       > 4
     OUTPUT
     tmux.until { assert_block(block, it) }
@@ -148,10 +148,10 @@ class TestLayout < TestInteractive
       │
       │   4
       │ > 3
-      │   2/2
-      │ >
       │   2
       │   1
+      │   2/2
+      │ >
       │   foo
       ╰───────
     OUTPUT
@@ -609,11 +609,11 @@ class TestLayout < TestInteractive
       │   4
       │ > 3
       ╰──────────
+          2
+          1
           98/98 ─
         >
       ╭──────────
-      │   2
-      │   1
       │   hello
       ╰──────────
     BLOCK
@@ -666,12 +666,12 @@ class TestLayout < TestInteractive
       │   4
       │ > 3
       ╰──────────
+          98/98 ─
+        >
       ╔══════════
       ║   2
       ║   1
       ╚══════════
-          98/98 ─
-        >
     BLOCK
     tmux.until { assert_block(block1, it) }