diff --git a/CHANGELOG.md b/CHANGELOG.md
index 9cc1af55..4e92620c 100644
--- a/CHANGELOG.md
+++ b/CHANGELOG.md
@@ -10,6 +10,10 @@ CHANGELOG
 
   # Separator shown; no border separates the input section from the list section
   fzf --style full --input-border none --header foo --no-header-border
+
+  # Conversely, separator is now shown when the input border does not draw
+  # a line facing the list section
+  fzf --input-border bottom
   ```
 - Rendering improvements
     - Each frame is now wrapped in synchronized update mode (mode 2026) to reduce flickering on supported terminals
diff --git a/src/options.go b/src/options.go
index f67583c9..39bda044 100644
--- a/src/options.go
+++ b/src/options.go
@@ -3699,7 +3699,14 @@ func (opts *Options) noSeparatorLine() bool {
 	// NOTE: This does not know that the default separator can be suppressed at
 	// runtime (see Terminal.separatorLength), so the minimum heights derived
 	// from it can be one line taller than strictly necessary.
-	sep := opts.Separator == nil && !opts.InputBorderShape.Visible() || opts.Separator != nil && len(*opts.Separator) > 0
+	//
+	// Whether the input border draws a line on the side facing the list
+	// section; BorderLine always resolves to that side (see NewTerminal)
+	shape := opts.InputBorderShape
+	facingLine := shape == tui.BorderLine ||
+		opts.Layout == layoutReverse && shape.HasBottom() ||
+		opts.Layout != layoutReverse && shape.HasTop()
+	sep := opts.Separator == nil && !facingLine || opts.Separator != nil && len(*opts.Separator) > 0
 	return noSeparatorLine(opts.InfoStyle, sep)
 }
 
diff --git a/src/terminal.go b/src/terminal.go
index a4815472..4425c48a 100644
--- a/src/terminal.go
+++ b/src/terminal.go
@@ -1714,7 +1714,9 @@ func (t *Terminal) separatorLength() int {
 // The default horizontal separator is redundant if the input section is
 // already visually separated from the list section by a border line
 func (t *Terminal) separatedByBorder() bool {
-	if t.inputBorderShape.Visible() {
+	// The input border itself draws a line on the side facing the list section
+	if t.layout == layoutReverse && t.inputBorderShape.HasBottom() ||
+		t.layout != layoutReverse && t.inputBorderShape.HasTop() {
 		return true
 	}
 	for po := &t.previewOpts; po != nil; po = po.alternative {
@@ -1727,7 +1729,7 @@ func (t *Terminal) separatedByBorder() bool {
 	}
 	hasHeaderLinesWindow, headerLinesShape := t.determineHeaderLinesShape()
 	hasHeaderWindow := t.hasHeaderWindow()
-	if !hasHeaderWindow && !hasHeaderLinesWindow {
+	if !t.inputBorderShape.Visible() && !hasHeaderWindow && !hasHeaderLinesWindow {
 		// No separate window is created for the input section in this case
 		// (see hasInputWindow in resizeWindows), i.e. the input section is
 		// embedded in the list window and no border separates the two
@@ -1736,7 +1738,11 @@ func (t *Terminal) separatedByBorder() bool {
 
 	// The input section has its own window. Determine which section it is
 	// facing, and check if the border of that section draws a line toward it.
-	if hasHeaderWindow && !t.headerFirst && t.headerBorderShape != tui.BorderInline {
+	// NOTE: hasHeaderWindow can be true with no header content when the input
+	// border is visible (see Terminal.hasHeaderWindow). An empty header window
+	// takes no space, so it cannot be the facing section.
+	hasHeaderSection := hasHeaderWindow && len(t.header0)+t.headerLines > 0
+	if hasHeaderSection && !t.headerFirst && t.headerBorderShape != tui.BorderInline {
 		// Header section; an inline header is not a separate section, it is
 		// drawn inside the list border, so it falls through to the branches
 		// below